Cardiac ImagingFree Access

Myocardial Tagging with MR Imaging: Overview of Normal and Pathologic Findings

Abstract

Magnetic resonance tagging is used to evaluate the dynamic deformation of lines or grids superimposed on the myocardium during the cardiac cycle. From these data, a specific postprocessing procedure provides two kinds of metrics: (a) three orthogonal components of myocardial motion (longitudinal, circumferential, and radial), and (b) rotation and torsion. Strain expresses the local myocardial deformation and is prone to important physiologic heterogeneities. Peak systolic strain is in the range of −15% to −20% for the longitudinal and circumferential components (fiber shortening) and 30%–40% for the radial component (wall thickening). The helical arrangement of myofibers that run in opposite directions at the epicardium and endocardium explains systolic twist (∼15°). This torsion may be enhanced during the early stage of several diseases (eg, hypertrophic cardiomyopathy) or in heart failure with a normal left ventricular ejection fraction. Strain is generally impaired in ischemic heart disease and cardiomyopathy, but the most diagnostically significant finding is the early identification of contractile dysfunction on the basis of longitudinal and circumferential strain reduction in patients with apparently preserved systolic function. Thus, strain impairment appears to be a sensitive and promising marker of subclinical disease, with the potential for improving patient management.

Introduction

The study of regional systolic left ventricular (LV) function is usually based on contour tracing, leading to overall contraction analysis (endocardial wall motion and wall thickening). However, this approach is limited to the assessment of radial displacement and thickening and can neither help differentiate between active and passive movements of myocardial segments (shortening) nor help evaluate myocardial rotation. Magnetic resonance (MR) tagging superimposes black lines or grids on the myocardium. The deformation of tracked tags in all directions throughout the cardiac cycle allows quantification of several objective (ie, operator-independent) hidden components of the motion. Ultrasonography (US)–based speckle tracking leads to similar possibilities of motion analysis and is comparable to MR tagging.

In this article, we discuss myocardial tagging with MR imaging in terms of basic principles, the main indexes derived from tagging data postprocessing, the main published results of the evaluation of various pathologic conditions, and potential clinical usefulness.

Principles of Myocardial Tagging with MR Imaging

Basic Concept

Myocardial tagging was introduced by Zerhouni et al (1) in 1988 and by Axel and Dougherty in 1989 (2).

Basically, black lines or grids are superimposed on and embedded in the myocardium at the beginning of a cine sequence, and the subsequent deformation of these lines throughout the cardiac cycle is noted (3)

. Special radiofrequency prepulses known as spatial modulation of magnetization (SPAMM) or DANTE (delays alternating with nutation for transient excitation) are applied just before the start of contraction (at the R wave of the electrocardiogram). CSPAMM (complementary SPAMM) represents an improvement on SPAMM and is aimed at providing sharper lines with better contrast.

Despite some fading effects (mainly during diastole) as time passes after the application of tags, alterations of this initial tagging pattern are relevant for several contraction properties (Fig 1). Because the myocardial T1 relaxation time is longer at 3.0 T (1100 msec) than at 1.5 T (900 msec), fading effect is less pronounced at higher field strengths. For the same reason, tagging is always performed prior to the injection of gadolinium-based contrast material.

Figure 1 Four-chamber views obtained in a 52-year-old patient with previous anterior infarction show grid deformation during the cardiac cycle (time elapsed after the R wave is indicated in each frame). Centripetal curvature of the lines is seen during systole in the normal myocardium (convexity oriented toward the center of the LV) (arrow), whereas akinetic regions demonstrate almost no grid deformation (arrowhead). During diastole, the contrast of the tagged lines progressively decreases (fading effect).

Acquisition is typically based on a prospective cine sequence; for example, all of the images in this article were obtained with 160 phase-encoding steps, a temporal resolution of 30 msec, and a breathhold spanning 18 heartbeats. Electrocardiographic gating with normal sinus rhythm is required for consistent results; image quality suffers greatly in cases of arrhythmia or if the patient is not able to hold the breath sufficiently. An intertag distance of 6 or 7 mm is typically used to obtain sufficient lines across the myocardial wall, the field of view is reduced as much as possible (eg, 280 mm), and a section thickness of 7–8 mm is used. A grid pattern is preferable to parallel lines because it allows analysis of both perpendicularly oriented components of myocardial deformation. The use of vertical and horizontal long axes and three short-axis sections (basal, equatorial, and apical) allows fairly good spatial sampling of the LV in the majority of cases. Compared with standard gradient-echo sequences, a steady-state free precession (SSFP) sequence provides sharper lines, improves contrast, and leads to better tag persistence (4).

Simple visual analysis of tag deformation is possible (Fig 1) and provides an immediate impression of the regional abnormal contraction pattern (eg, during a dobutamine stress test), with greater discrimination capabilities than are available with basic cine views.

However, the postprocessing procedures open the door to much more interesting quantitative analysis. This analysis may be performed on the reconstructed image itself using optical flow or some other tracking algorithm; however, this approach is quite cumbersome compared with the more convenient automatic (operator-independent) harmonic phase analysis method described by Osman et al (5). Harmonic phase analysis is based on a specific processing algorithm (tracking of phase change from one of the off-center spectral peaks) in the k-space domain. Several softwares are available that make use of this method. All of the images in this article were obtained with InTag software (www.creatis.insa-lyon.fr/inTag/). In practice, the time required for each tagging sequence is approximately 15–20 seconds for acquisition and 3–4 minutes for postprocessing (on a remote computer).

Components of Strain

Strain (ie, deformation) refers to the change in shape resulting from contraction and is expressed (as a percentage) as the fractional change in the length L of an elementary myocardial segment in a given direction during the cardiac cycle (ΔL/L) (Fig 2)

. It is important to distinguish between displacement (which may reflect a passive tethering effect) and strain (which involves a change in the distance between two distinct tag points, thereby reflecting an active process). Lengthening (stretch) yields positive strain values, whereas shortening yields negative strain values.

Figure 2 Images obtained during diastole (left) and systole (right) (magnified views shown at bottom) demonstrate the definition of strain (expressed as a percentage) as Δ*L/L*₀, where L = length of an elementary myocardial segment and ΔL = *L−L*₀. Red lines represent radial strain measurements (red segments are oriented radially, or toward the center of the LV), green lines represent circumferential strain measurements (green segments are oriented tangential to the myocardial wall, along its perimeter).

Basically, the two mathematic vectors of strain are called maximal and minimal principal strains and are defined according to the direction of the main myofibers. However, for the purposes of gaining a better clinical understanding of these phenomena, in-plane components of strain are recalculated relative to the main direction of the LV (local cardiac coordinate).

In a short-axis plane, the two orthogonal vectors are (a) radial strain (oriented toward the central long axis of the LV) and (b) circumferential strain (tangential to the epicardial wall). In a long-axis plane, the two orthogonal vectors are (a) radial strain (oriented toward the center of the LV, which should be the same as when viewed in a short-axis plane), and (b) longitudinal strain (tangential to the myocardial wall) (Figs 3, 4).

Figure 3 Drawing illustrates the three types of strain obtained from tagging data. In the long-axis plane, the systolic longitudinal deformation corresponds to apex-base shortening. In the short-axis plane, circumferential strain is tangential to the epicardial wall (oriented along the perimeter), and radial strain is oriented toward the center of the LV cavity. When viewed from the apex, sections close to the apex have a counterclockwise systolic rotation, whereas sections close to the base have a clockwise rotation.

Figure 4 Drawings illustrate how circumferential and radial strains are obtained from short-axis sections, whereas longitudinal strain is obtained from long-axis sections. Cd = circumferential strain in diastole, Cs = circumferential strain in systole, Ld = longitudinal strain in diastole, Ls = longitudinal strain in systole, Rd = radial strain in diastole, Rs = radial strain in systole.

Normal strain values (Table) within the myocardium are quite heterogeneous, but overall averaged values have been reported in several studies (6,7) and are almost identical to the values derived with the speckle tracking technique. Radial strain is in the 30%–40% range during systole and reflects wall thickening toward the center of the LV (6,7). Because the epicardial contour shows only limited motion, radial thickening is mainly expressed by endocardial motion, which is usually well appreciated visually and corresponds to the thickening seen at two-dimensional or M-mode echocardiography. With tagging, the direct measurement of radial strain is relatively imprecise, since a small number of tags span the myocardial wall (7). Therefore, radial strain cannot be measured as reproducibly as wall thickening.

Normal longitudinal and circumferential strains both range from −15% to −20% during systole and reflect shortening of the myocardial fibers during systole.

For example, Kuijer et al (6) and Moore et al (7) found ranges of −16% to −21% and −18% to −23%, respectively. Longitudinal strain corresponds to motion toward the apex (base-to-apex shortening with an accordion-like movement) and may be roughly assessed visually on long-axis views. This component has been the most studied and has emerged as the most useful at US speckle tracking. Circumferential strain has a significance similar to that of longitudinal strain (fiber shortening) but cannot be appreciated visually (Fig 5 ). Because the contraction of the sarcomeres occurs along the myofibers, the active contraction is only longitudinal and circumferential, whereas radial thickening is not a primary phenomenon but is only a consequence of fiber rearrangement.

Circumferential strain. (a) Midventricular short-axis section illustrates a systolic circumferential vector field (red). (b) Short-axis section with a superimposed color parametric map illustrates high strain values (blue) and weak strain values (yellow). (c) Graph illustrates circumferential strain curves obtained in six myocardial sectors. Each curve corresponds to a specific regional contraction pattern and is color coded for clarity. Strain distribution is heterogeneous. Along the radial direction, values are higher in the subendocardial layer (−40% to −30%) than in the subepicardial layer (−10% to −20%). Septal strain is weaker than lateral or anterior (ant) strain. (Average peak strain in healthy individuals = −18% ± 2.) Inf = inferior.

**Strain Parameters in Normal and Pathologic Conditions**

HFNEF = heart failure with normal ejection fraction and includes other diseases with subclinical systolic dysfunction.

^*Clockwise.

^†Counterclockwise.

Diastolic indexes may also be obtained with MR tagging. However, because the T1-related fading phenomenon increases the noise level in the measurement, the reproducibility of MR diastolic indexes is lower than that of diastolic indexes obtained with speckle tracking. Strain rate is the derivative of strain (expressed as 1/sec) and reflects the speed of deformation, but this index is highly sensitive to noise.

These components of strain may be expressed in several ways—for example, as a time-intensity curve, which illustrates variation during the cardiac cycle; dynamic vector fields superimposed on the anatomic image; or a dynamic parametric map, with each magnitude of the strain encoded in a specific color (Fig 5).

Moreover, it is possible to combine several strain components into a synthetic composite index. For example, a multiparametric z-score map may be constructed (8), allowing visual assessment of a normal or abnormal segmental contraction pattern.

One must keep in mind that all of these functional indexes are affected by the loading conditions. However, unlike displacement and velocity, the strain indexes are not influenced by bulk motion, passive tethering, or translation.

Assessment of Cardiac Dyssynchrony

Intraventricular dyssynchrony may be expressed in many ways—for example, as the dispersion of the time-to-peak intervals in each segmental contraction curve—and has been studied for years, largely with radionuclide ventriculography, Doppler tissue imaging, and speckle tracking. Parametric time-to-peak maps are useful for detecting focal dyskinetic motion after myocardial infarction or in right ventricular (RV) arrhythmogenic dysplasia. Standard deviation (SD) of the time to peak obtained with MR tagging (Fig 6) quantifies dyssynchrony and is altered mainly in the left bundle branch block (LBBB) and ventricular aneurysm. However, several other indexes may be computed from the segmental contraction curve (eg, strain variance, phase dispersion derived from Fourier analysis, calculation of the amount of energy loss with the “strain delay index” [9]), and there is not yet a general consensus regarding a universal marker of ventricular dyssynchrony.

Figure 6 Graph illustrates a series of circumferential strain curves obtained in different segments and offers several possibilities for quantifying dyssynchrony. Here, the SD of the time to peak (short vertical line on each curve) is 17 msec and is calculated from the circumferential strain curves obtained in 12 sectors in an apical short-axis section.

Rotation and Torsion Related to the Complex Architecture of Myocardial Fibers

Early anatomic representations of the heart clearly showed the oblique curvilinear arrangement of the myocardial fibers (Fig 7a). Histologic studies concerning three-dimensional architecture of the myocardial fibers (10), and more recent studies based on diffusion MR tractography (11), have confirmed a complex multilayered helical layout. The oblique orientation of subepicardial myocardial fibers (which course from the upper left base to the bottom right apex when the heart is viewed anteriorly) is perpendicular to the oblique orientation of fibers in the subendocardial layer, whereas midwall fibers, which are the most numerous, are oriented transversely (Fig 3). This perpendicular arrangement is explained by the helical reflection of a single continuous myocardial band according to the muscle band theory (Fig 7b) (12,13).

(a) Drawing illustrates the oblique arrangement of myocardial fibers as depicted in Anatomie et Physiologie Animale by Mathias Duval, a textbook published in 1890 for the preparation of the bachelor. The caption for the figure reads, “Path of the muscle fibers at the apex of the heart.” The corresponding text says, “The fibers take their origin at the base of the ventricle, are going through the apex of the heart, and form a loop to go back to the wall of the other ventricle.” (Reproduced, with permission, from Bibliothèque Inter Universitaire de Médecine à Paris.) (b) Drawing illustrates the concept of the muscle band theory as presented by Torrent-Guasp, with one single continuous band of myofibers extending from the pulmonary artery up to the aortic root (broken lines and arrowheads). (Adapted, with permission, from reference 12.)

For each cardiac phase, the rotation at each myocardial point is calculated as the angle around the axis of rotation relative to the position during end-diastole. The definition of the axis of rotation (fixed or moving) may vary from one study to another. Averaging the value at all myocardial points yields the global mean rotation. Twist is calculated as the difference between the apical and basal rotations. Torsion may be defined similarly to twist but may also be defined as twist divided by long-axis length (twist per unit length), or as the circumferential-longitudinal shear angle (twist times the quotient of mean radius and length between the apical and basal planes) (14).

When the heart is viewed from the apex, systolic rotation is clockwise at the base and counterclockwise at the apical level (Figs 3, 8). The direction of twist is consistent with the arrangement of epicardial fibers because of the greater epicardial muscle mass and a greater moment arm about the long axis (7). It is as if one were to hold the heart base with the left hand, the apex with the right hand, and twist as if unscrewing a cap or opening a valve (counterclockwise if the apex is in the foreground). At the end of systole, the opposite motion (untwist or recoil) occurring during the isovolumic period seems to be an important determinant of ventricular filling (ie, twist could be considered as a kind of energy storage mechanism). These data, corroborated by speckle tracking studies, have been extensively described by Buckberg et al (12). These rotational movements are more pronounced in the subendocardium than in the subepicardium and range from −4° to −7° at the base (clockwise) and from 5° to 10° at the apex (counterclockwise). The difference between rotation at the base (negative angle) and rotation at the apex (positive angle) is twist (range, 10°–15°).

Figure 8 Short-axis sections obtained at the base and apex of the heart in a healthy subject and corresponding graphs illustrate clockwise versus counterclockwise rotation. Red lines on images = displacement field vectors. On the basal section, displacement vectors are curved clockwise with a very heterogeneous rotation (almost absent in the septum). On the apical section, vectors are curved counterclockwise with a much more homogeneous rotation (∼11° in this case). Colored lines on graphs indicate the curves of the angle of rotation in six myocardial sectors.

Physiologic Heterogeneity of the Strain

Strain heterogeneities revealed by tagging have been described in several review articles (6,7,15,16).

1.	As one moves from the base to the apex, the circumferential and longitudinal strains increase, whereas the downward base motion is greater than apical rising (the apex pulls the ventricular base down with a tethering movement). This apparent discrepancy highlights the fact that the passive tethering motion (higher at the base) does not reflect the true active contraction phenomenon expressed by strain (higher at the apex).
2.	As one moves from the epicardium to the endocardium, the circumferential, longitudinal, and radial strains (as well as torsion) increase.
3.	The circumferential and longitudinal strains are greater in the lateral wall and lesser in the septum.
4.	Contraction begins in the lateral wall, whereas the septum is the last part to be activated. Conversely, the peak of contraction is initially reached by the septum (shorter contraction time), and then by the lateral wall.
5.	Rotation and torsion are greater and more prolonged in elderly patients (15). The large Multi-Ethnic Study of Atherosclerosis also found significant differences in circumferential strain among various ethnic groups (17); for example, greater magnitude was found in Chinese Americans (−19.60% ± 3.78), whereas lesser magnitude was found in African Americans (−17.50% ± 4.00, P < 0.05).

Tagging versus Other Techniques

Methods other than tagging have also been proposed for the quantification of regional deformation.

The US-based speckle tracking technique is more widely used than MR tagging and can now be a part of routine echocardiography, thanks to its wide availability and ease of use (unlike with MR tagging, the data are processed online and in real time). For this reason, more published clinical studies are based on speckle tracking than on MR tagging. Direct comparisons (18–20) have shown the normal range and regional heterogeneity of the two techniques to be quite similar, although slightly higher values may be found with speckle tracking (such small differences may also be observed within the tagging studies when certain postprocessing software is used). Overall, the analysis of circumferential strain appears to be easier with MR tagging than with US speckle tracking, whereas radial strain is better assessed with speckle tracking owing to the limited number of tags spanning the myocardial wall with MR tagging.

Recently, a promising concept known as feature tracking was introduced. This technique is comparable to speckle tracking as used in echocardiography, but so far it has been useful only for the evaluation of epicardial or endocardial borders (but not midwall layers). The strength of this method, which compares favorably with tagging (21), is that it relies on the basic cine MR sequences without any need for a specific encoding pulse.

Displacement-encoded with stimulated-echo (DENSE) imaging is an interesting phase-based MR method (22). Like MR tagging, DENSE imaging provides functional maps of local motion (Fig 9 ). Tissue velocity in each pixel may be encoded in three dimensions (ie, even in the through-plane direction), and the technique may be implemented during free breathing (navigator based). A key feature of this technique is that it relies on pixel-wise spatial resolution, without the need for interpolation methods as in tagging. The direct clinical applicability of DENSE imaging explains why this technique may supplant MR tagging in the coming years. However, it is not widely available at present.

Reperfused acute inferoseptal myocardial infarction in a 56-year-old man. (a) Basal short-axis section demonstrates transmural late enhancement with a small area of no reflow. (b) Cine DENSE end-systolic parametric map of the circumferential strain (Ecc) shows abnormal deformation in the inferoseptal regions (blue), despite inward motion as displayed by the displacement vectors (curved lines) for each of the pixels. (c) Graph illustrates deformation curves with reduced circumferential strain (Ecc) magnitude in the corresponding inferior and inferoseptal sectors.

Myocardial Tagging in the Evaluation of Cardiac Diseases

Ischemic Heart Disease

MR tagging–derived strains provide useful objective quantitative indexes that are superior to the simple visual assessment of LV motion abnormalities and improve the diagnostic performance of a dobutamine stress test for the detection of coronary heart disease in patients with complaints of chest pain (23).

This is because visual analysis relies mainly on systolic inward motion, whereas tagging allows the evaluation of longitudinal or circumferential shortening that is barely visible to the naked eye.

After myocardial infarction, all components of strain are decreased or even inverted (stretching instead of shortening in dyskinetic area) (Fig 10 ) (24). Moreover, the strain alteration is greater than the wall thickening alteration and allows better discrimination between normal and infarcted myocardium (25). After myocardial infarction, apical rotation and torsion are decreased, but this change is weaker than the alteration of segmental wall shortening.

Inferior wall infarction in a 64-year-old patient. LV end-diastolic volume index (LVEDVI) = 91 mL/m² (normal value < 95 mL/m²), LV ejection fraction (LVEF) = 49%. (a–c) SSFP short-axis cine MR images obtained during diastole (a) and systole (b) and phase-sensitive inversion recovery image (c) show inferior akinesia in the region of gadolinium-induced late enhancement. (d–f) Color maps superimposed on basal (d), middle (e), and apical (f) images show circumferential strain and allow better quantification of the magnitude and extent of the segmental contraction abnormality. Yellow-red segments indicate reduced fiber shortening and even a pathologic systolic stretch.

In patients with chronic ischemic LV dysfunction, the increase in strain and strain rate with low-dose dobutamine administration is a marker of myocardial viability, and MR tagging has proved to be useful in this setting (26). In cases of small subendocardial myocardial infarction, strain analysis seems to be more sensitive than endocardial wall motion or wall thickening (Fig 11 ).

Small anterior-basal subendocardial non–ST-segment elevation myocardial infarction in a 37-year-old man. Troponin I = 2.3 μg/L, LVEDVI = 77 mL/m² (normal value < 95 mL/m²), LVEF = 59%. (a–c) SSFP long-axis cine MR images obtained during diastole (a) and systole (b) and after gadolinium administration (c) show no segmental wall motion abnormality (arrowhead in c). (d, e) Short-axis tagged image (d) and corresponding graph (e) clearly show lack of systolic grid deformation in the anterior basal wall, with a marked reduction in maximum circumferential strain magnitude (arrowhead). The average peak strain magnitude is slightly reduced (−15.4% ± 5.8) (normal range, −18% ± 2).

Cardiac resynchronization therapy (CRT) is indicated to improve contraction synchronism in heart failure patients with a low LVEF and wide QRS complex (>120 msec). In addition to Doppler tissue imaging and speckle tracking indexes, MR tagging dyssynchrony metrics have been proposed to help better identify optimal responders to CRT (the greater the dyssynchrony, the greater the functional improvement after CRT). In an animal study by Helm et al (27) in which several indexes reflecting temporal uniformity or regional strain variance were used, circumferential strain was more predictive in terms of this issue than was longitudinal strain (which is usually used in US studies). In a clinical study, Bilchick et al (28) showed that the circumferential mechanical dyssynchrony index could help predict improved function after CRT with 90% accuracy (much better than with the classic Doppler imaging septal-lateral delay).

Dilated Cardiomyopathy

Reduced wall motion and dyssynchrony are the hallmarks of hypokinetic dilated cardiomyopathies. The strain abnormalities demonstrate marked spatial heterogeneity (Fig 12 ). For example, circumferential shortening was found to be less than one-third of the normal value in dilated cardiomyopathy as compared with healthy patients (−5.3% ± 2.1 versus −18.6% ± 2.9) (29). Systolic stretch is often observed instead of normal shortening of the septum, whereas lateral wall strain is relatively preserved. Base-apex twist is reduced by approximately one-half and becomes prematurely interrupted in early systole as compared with the normal heart (30).

Cardiac failure related to dilated cardiomyopathy in a 66-year-old man with normal coronary angiographic findings. LVEDVI = 147 mL/m² (normal value < 95 mL/m²), LVEF = 20%, LV mass index (LVMI) = 115 g/m² (normal value < 92 g/m²). (a, b) Horizontal (a) and short-axis (b) SSFP systolic cine MR images show an enlarged LV. (c–f) Short-axis section (c), corresponding graph (d), and short-axis sections with color coding (e, f) created for circumferential strain analysis demonstrate abnormal septal stretching and a markedly reduced overall systolic strain magnitude of −4% ± 6 (normal range, −18% ± 2).

LBBB is present in at least 25% of these patients and leads to deleterious septal hypoperfusion and LV remodeling. LBBB worsens the contraction abnormalities and dyssynchrony and is a predictor of poor outcome. In 50% of patients with LBBB (either related or unrelated to ischemic disease), strain studies have demonstrated that dyskinesia of the inferior or anteroseptal wall is preceded by a small systolic early contraction (preejectional flash) (31). Dyskinesia of the anteroseptal wall is seen in 30% of cases (Fig 12), and a simple hypokinesia is seen in the remaining 20%. Circumferential strain magnitude is similarly reduced in dilated cardiomyopathies with or without LBBB, but dyssynchrony is markedly increased in cases of LBBB (maximal contraction time-to-peak SD = 164 msec [versus 70 msec when LBBB is absent]). The loss of opposite LV basal and apical rotation is predictive of an acute response to CRT and is associated with LV reverse remodeling (32).

Hypertrophic Cardiomyopathy

In hypertrophic cardiomyopathy, despite apparently normal global LV function, circumferential septal strain magnitude is significantly reduced (−13.4% ± 4.7 versus −19.5% ± 2.3) (Figs 13 , 14 ), and diastolic strain is reduced in all territories (33). Dyssynchrony indexes and apical rotation are increased (15,16). The strain alteration predominates in fibrous areas, manifesting as late enhancement after gadolinium injection (seen in more than 80% of patients with hypertrophic cardiomyopathy), mostly at the upper part of the thickened septum connecting to the RV. This alteration may also manifest as small nodular foci showing late enhancement within nonhypertrophic areas. Strain assessment is also useful in differentiating between so-called athlete’s heart (physiologic hypertrophy with normal strain values) and asymptomatic nonobstructive hypertrophic cardiomyopathy or hypertensive cardiac hypertrophy (34).

Restrictive heart failure with amyloidosis-related concentric hypertrophic cardiomyopathy in an 82-year-old woman. (a) SSFP short-axis cine MR image shows diastolic septal thickening (24 mm). LVEDVI = 65 mL/m² (normal value < 92 mL/m²), LVEF = 64%, LVMI = 203 g/m² (normal value < 88 g/m²). (b, c) Tagged images show markedly reduced septal motion (b) and circumferential strain magnitude (c) (−10% ± 6; normal range, −18% ± 2). (d) Gadolinium-enhanced MR image shows circumferential subendocardial enhancement predominantly in the basal region. (e) Graph illustrates markedly reduced circumferential strain magnitude (cf c).

Predominantly septal hypertrophic cardiomyopathy in a 57-year-old man. LVEDVI = 72 mL/m² (normal value < 95 mL/m²), LVEF = 83%, LVMI = 138 g/m² (normal value < 90 g/m²). (a) SSFP short-axis cine MR image shows marked septal hypertrophy. (b) Tagged image shows total lack of motion and grid deformation within the thickened septum. (c–e) Circumferential strain map (c), gadolinium-enhanced MR image (d), and corresponding graph (e) help confirm abnormal contraction pattern, mainly in the lower part of the septum, which is infiltrated by fibrotic tissue (hyperenhanced area in d).

Aortic Stenosis

Apical rotation is increased in aortic stenosis (22.2° ± 5.9 versus 10.3° ± 2.5) (35); base-apex torsion is also increased but normalizes 1 year after aortic valve replacement. Untwisting prior to LV filling is prolonged. Such abnormal patterns are not seen in athletes with myocardial hypertrophy (36).

HFNEF and Other Diseases with Subclinical Systolic Dysfunction

HFNEF is characterized by (a) symptoms of congestive heart failure, (b) normal or mildly abnormal systolic LV function (LVEF > 50), and (c) evidence of abnormal LV filling (37). HFNEF is an important issue because it accounts for 40%–50% of all causes of heart failure, and its morbidity and mortality rates are similar to those for heart failure related to systolic dysfunction. Imaging features that are typically used to identify HFNEF include myocardial wall hypertrophy, an enlarged left atrium, and LV filling abnormalities. Two kinds of tagging-derived indexes have been studied with respect to this issue: strain and rotation.

Strain.—Global longitudinal strain, mainly studied with speckle tracking (38) and having been reported as the most relevant index, is significantly reduced despite preserved LVEF. Increased radial strain is thought to be a “compensatory” mechanism for preserved LVEF in HFNEF patients with LV hypertrophy.

As for HFNEF, the identification of strain disturbance (with systolic function seemingly preserved) is a decisive step toward revealing hidden heart damage in many pathologic conditions (Fig 15 ).

For example, a reduction in circumferential strain allows the detection of occult cardiac dysfunction in Duchenne muscular dystrophy despite preserved LVEF (39). The large Multi-Ethnic Study of Atherosclerosis showed that among asymptomatic individuals without clinical cardiovascular disease, an elevated fibrinogen level is independently associated with a reduction in absolute circumferential strain in all regions (40). With use of speckle tracking, global longitudinal strain reduction has also been found to be a subclinical marker of occult myocardial dysfunction in various diseases, including diabetes (41), early-stage chronic kidney disease (42), doxorubicin-induced toxicity (43), cardiac transplant rejection (34), and hypertension with concentric LV hypertrophy (∼20% of the strain magnitude reduction) (44). Moreover, global longitudinal strain is a better predictor of forthcoming major cardiac events than is LVEF (45).

Restrictive cardiac failure due to amyloidosis in a 64-year-old man who presented with congestive signs. LVEDVI = 75 mL/m² (normal value < 95 mL/m²), LVEF = 65%, LVMI = 168 g/m² (normal value < 90 g/m²). (a, b) Diastolic (a) and systolic (b) SSFP long-axis cine MR images. (c, d) Graph (c) and color-coded tagged image (d) created for longitudinal strain analysis show severely impaired strain values except at the apical level, despite apparently normal systolic function (average longitudinal strain, −6% ± 5).

Rotation.—Rotation and torsion alterations show a biphasic pattern during the course of diastolic dysfunction, with an initial increase in systolic twist and a return to normal values—or even a decrease—in moderate or severe diastolic dysfunction (46,47). Such alterations in systolic torsion might be compared to the biphasic time course of transmitral flow profile alterations (abnormal relaxation profile and further pseudonormalization) in patients with diastolic dysfunction. Increased torsion in early-stage HFNEF is similar to age-related changes (46,48) and to subclinical alterations observed in hypertrophic cardiomyopathy mutation carriers with normal wall thickness (49). Increased torsion could reflect some dysfunction of the subendocardial myofibers, which normally counteracts the LV twisting generated by the subepicardial myofibers (50). Reduction of the physiologic delay between the time to peak basal rotation and the time to peak apical rotation (which occurs earlier) could also help explain the enhanced torsion in these patients (46).

Diseases Involving the Right Heart

In constrictive pericarditis, the adhesion between the layers of the pericardium prevents the normal shearing of tagged stripes across the pericardium (51).

RV tagging is difficult owing to the thin wall of the RV (<5 mm, which is less than the optimal tag spacing). However, it has been demonstrated that the magnitude of RV circumferential and longitudinal strain is reduced in pulmonary hypertension, and prolonged RV systolic contraction leads to an interventricular mechanical delay (time to peak = 293 msec ± 58 for the LV versus 387 msec ± 50 for the RV) (52). Conversely, strain may be preserved despite the abnormal wall motion pattern. For example, the “paradoxical septal motion” observed in RV overload (Fig 16 ) or after heart surgery with pericardiotomy may be associated with normal circumferential strain. Choi et al (53) reported that septal strain remained normal after coronary artery bypass graft surgery, whereas septal motion was altered in 56% of patients. This means that abnormal septal motion was not due to ischemia, but rather was related to increased anterior cardiac mobility after the pericardial incision was made.

Paradoxical septal motion in a 38-year-old man who had undergone pulmonary valvuloplasty in early childhood. The patient presented with valvular pulmonary stenosis (G_max = 63 mm Hg) and regurgitation (regurgitant fraction = 40%). Right EDVI = 182 mL/m² (normal value < 110 mL/m²), RV ejection fraction = 57%. (a, b) SSFP short-axis cine MR images obtained during diastole (a) and systole (b) show a markedly enlarged RV with a thickened anterior free wall. (c) Displacement field map shows anterior bulk movement of the entire LV (arrow) during systole, leading to the typical finding of paradoxical septal motion. (d, e) On short-axis sections obtained during diastole (d) and systole (e), RV systolic function remains good and the systolic curvature of the tagged lines is normal. Moreover, normal septal thickening is seen to occur during systole. (f) Circumferential strain map demonstrates preserved contraction of the LV walls.

Conclusions

Although the wider availability of MR tagging sequences and postprocessing software has made tagging operational, its implementation is less straightforward than that of US speckle tracking. Tagging offers numerous new metrics for improved analysis of LV function relative to strain, rotation, and dyssynchrony. Many physiologic and pathologic features have already been described. At present, the most interesting indexes rely on strain magnitude reduction despite apparently normal systolic function. Thus, MR tagging can be described as a kind of “magnifying glass” that allows access to useful data that have remained hidden up until now. This advantage may have important applications in several situations with preserved LVEF (eg, ischemic, hypertensive, valvular, metabolic, or systemic diseases) or in the early detection of chemotherapy-related toxicity. However, it must be recognized that as long as strain values are not available online (at least not through a convenient and rapid postprocessing step, such as for calculation of LVEF), MR tagging will remain confined to research laboratories and will be difficult to use in routine clinical practice.

Disclosures of Potential Conflicts of Interest.—P.C.:Related financial activities: none. Other financial activities: speaker for Siemens, Guerbet, and Novartis.

The authors thank Joost P. A. Kuijer, PhD, VU University Medical Center, Amsterdam, the Netherlands, for developing and providing the CSPAMM tagging package (work-in-progress); and Patrick Clarysse of CREATIS-LRMN, INSA Lyon, University of Lyon, Villeurbanne, France, for providing the postprocessing InTag software and useful advice.

Presented as an education exhibit at the 2010 RSNA Annual Meeting

P.C. has disclosed various financial relationships (see “Disclosures of Potential Conflicts of Interest”); all other authors, the editor, and reviewers have no financial relationships to disclose.

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Article History

Received: Apr 20 2011
Revision requested: Aug 25 2011
Revision received: Feb 6 2012
Accepted: Apr 30 2012
Published online: Aug 31 2012
Published in print: Sept 2012

Vol. 32, No. 5

Abbreviations

Abbreviations:
CRT	cardiac resynchronization therapy
DENSE	displacement-encoded with stimulated-echo
HFNEF	heart failure with normal ejection fraction
LBBB	left bundle branch block
LV	left ventricle
LVEDVI	LV end-diastolic volume index
LVEF	LV ejection fraction
LVMI	LV mass index
RV	right ventricle
SPAMM	spatial modulation of magnetization
SSFP	steady-state free precession

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