Objectives To compare a steady-state free precession cine sequence-based technique (feature tracking [FT]) to tagged harmonic phase (HARP) analysis for peak average circumferential myocardial strain (epsilon(cc)) analysis in a large and heterogeneous population of boys with Duchenne muscular dystrophy (DMD). Background Current epsilon(cc) assessment techniques require cardiac magnetic resonance-tagged imaging sequences, and their analysis is complex. The FT method can readily be performed on standard cine (steady-state free precession) sequences. Methods We compared mid-left ventricular whole-slice epsilon(cc) by the 2 techniques in 191 DMD patients grouped according to age and severity of cardiac dysfunction: group B: DMD patients 10 years and younger with normal ejection fraction (EF); group C: DMD patients older than 10 years with normal EF; group D: DMD patients older than 10 years with reduced EF but negative myocardial delayed enhancement (MDE); group E: DMD patients older than 10 years with reduced EF and positive MDE; and group A: 42 control subjects. Retrospective, offline analysis was performed on matched tagged and steady-state free precession slices. Results For the entire study population (N = 233), mean FT epsilon(cc) values (-13.3 +/- 3.8%) were highly correlated with HARP epsilon(cc) values (-13.6 +/- 3.4%), with a Pearson correlation coefficient of 0.899. The mean epsilon(cc) of DMD patients determined by HARP (-12.52 +/- 2.69%) and FT (-12.16 +/- 3.12%) was not significantly different (p = NS). Similarly, the mean epsilon(cc) of the control subjects by determined HARP (-18.85 +/- 1.86) and FT (-18.81 +/- 1.83) was not significantly different (p = NS). Excellent correlation between the 2 methods was found among subgroups A through E, except there was no significant difference in strain between groups B and C with FT analysis. Conclusions FT-based assessment of epsilon(cc) correlates highly with epsilon(cc) derived from tagged images in a large DMD patient population with a wide range of cardiac dysfunction and can be performed without additional imaging.

Comparison of Magnetic Resonance Feature Tracking for Strain Calculation With Harmonic Phase Imaging Analysis

Cardiovascular magnetic resonance (CMR) creates images from atomic nuclei with uneven spin using radiowaves in the presence of a magnetic field. Full details of the physical principles can be found elsewhere.1 For clinical purposes, MR is performed using hydrogen-1, which is abundant in water and fat. Radiofrequency waves excite the area of interest to create tissue magnetization that decays (relaxation) and after a short period is induced to release energy as a radio signal. These echoes are converted with Fourier transformation into images of spatially resolved radio signals. Relaxation is quantified in spatially orthogonal directions as T1 and T2, which allows tissue characterization to serve as a powerful clinical tool. A CMR scanner consists of a superconducting magnet, a radiofrequency transmitter and receiver connected to radio aerials, and gradient coils driven by powerful pulses of electricity to create transient magnetic fields. The imaging computer triggers to the ECG and runs scanning sequences that coordinate the complex processes. The spin-echo sequence yields static images with black blood, whereas the gradient-echo sequence usually acquires multiple images through the cardiac cycle that display cardiovascular function as cine loops. Preparation pulses can be used to display T1 or T2 contrast for tissue characterization. Fast and real-time sequences include fast low-angle shot, steady-state free-precession, spiral, and echo-planar imaging. Velocity and flow can be quantified with gradient-echo sequences with encoding of velocity in the signal phase.2

CMR is extremely safe, which is unequivocally advantageous compared with x-rays, but special cautions apply. Ferromagnetic items become potentially dangerous projectiles in the scanner room. Although most metallic medical implants, including all prosthetic cardiac valves and coronary stents, are MR compatible, care is required with cerebrovascular clips. Pacemakers and defibrillators present problems, in particular related to wire heating, and are a contraindication for CMR, although specialist centers have …

Cardiovascular Magnetic Resonance

Cardiovascular magnetic resonance (CMR) tagging has been established as an essential technique for measuring regional myocardial function. It allows quantification of local intramyocardial motion measures, e.g. strain and strain rate. The invention of CMR tagging came in the late eighties, where the technique allowed for the first time for visualizing transmural myocardial movement without having to implant physical markers. This new idea opened the door for a series of developments and improvements that continue up to the present time. Different tagging techniques are currently available that are more extensive, improved, and sophisticated than they were twenty years ago. Each of these techniques has different versions for improved resolution, signal-to-noise ratio (SNR), scan time, anatomical coverage, three-dimensional capability, and image quality. The tagging techniques covered in this article can be broadly divided into two main categories: 1) Basic techniques, which include magnetization saturation, spatial modulation of magnetization (SPAMM), delay alternating with nutations for tailored excitation (DANTE), and complementary SPAMM (CSPAMM); and 2) Advanced techniques, which include harmonic phase (HARP), displacement encoding with stimulated echoes (DENSE), and strain encoding (SENC). Although most of these techniques were developed by separate groups and evolved from different backgrounds, they are in fact closely related to each other, and they can be interpreted from more than one perspective. Some of these techniques even followed parallel paths of developments, as illustrated in the article. As each technique has its own advantages, some efforts have been made to combine different techniques together for improved image quality or composite information acquisition. In this review, different developments in pulse sequences and related image processing techniques are described along with the necessities that led to their invention, which makes this article easy to read and the covered techniques easy to follow. Major studies that applied CMR tagging for studying myocardial mechanics are also summarized. Finally, the current article includes a plethora of ideas and techniques with over 300 references that motivate the reader to think about the future of CMR tagging.

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Myocardial tagging by Cardiovascular Magnetic Resonance: evolution of techniques--pulse sequences, analysis algorithms, and applications

Structural remodeling of myocardium after infarction plays a critical role in functional adaptation. Diffusion tensor magnetic resonance imaging (DTMRI) provides a means for rapid and nondestructiv...

https://www.physiology.org/doi/pdf/10.1152/ajpheart.00889.2002

Remodeling of cardiac fiber structure after infarction in rats quantified with diffusion tensor MRI

Dynamic changes of myocardial fiber and sheet structure are key determinants of regional ventricular function. However, quantitative characterization of the contraction-related changes in fiber and sheet structure has not been reported. The objective of this study was to quantify cardiac fiber and sheet structure at selected phases of the cardiac cycle. Diffusion tensor MRI was performed on isolated, perfused Sprague-Dawley rat hearts arrested or fixed in three states as follows: 1) potassium arrested (PA), which represents end diastole; 2) barium-induced contracture with volume (BV+), which represents isovolumic contraction or early systole; and 3) barium-induced contracture without volume (BV-), which represents end systole. Myocardial fiber orientations at the base, midventricle, and apex were determined from the primary eigenvectors of the diffusion tensor. Sheet structure was determined from the secondary and tertiary eigenvectors at the same locations. We observed that the transmural distribution of the myofiber helix angle remained unchanged as contraction proceeded from PA to BV+, but endocardial and epicardial fibers became more longitudinally orientated in the BV- group. Although sheet structure exhibited significant regional variations, changes in sheet structure during myocardial contraction were relatively uniform across regions. The magnitude of the sheet angle, which is an index of local sheet slope, decreased by 23 and 44% in BV+ and BV- groups, respectively, which suggests more radial orientation of the sheet. In summary, we have shown for the first time that geometric changes in both sheet and fiber orientation provide a substantial mechanism for radial wall thickening independent of active components due to myofiber shortening. Our results provide direct evidence that sheet reorientation is a primary determinant of myocardial wall thickening.

Regional ventricular wall thickening reflects changes in cardiac fiber and sheet structure during contraction: quantification with diffusion tensor MRI.

Purpose

To examine the relationship between myofiber disarray and myocardial hypokinesis in human hypertrophic cardiomyopathy (HCM) using noninvasive cardiac diffusion and strain MRI.



Materials and Methods

Five patients with a diagnosis of HCM and five age-matched healthy volunteers were studied and compared. Cardiac diffusion MRI was applied to map in vivo myocardial fiber architecture. Cardiac strain MRI was applied to map myocardial motion. By acquiring registered diffusion and strain MRI images in vivo on both normal and HCM hearts, we investigated in HCM the relationship between myofiber disarray and systolic strain components, including radial, fiber, and cross-fiber strains, and sought to determine the mechanism behind disarray-related myocardial dysfunction in HCM.



Results

Regionally disordered fiber orientation and reduced diffusion fractional anisotropy (FA) were found in HCM, demonstrating myofiber disarray. Intramural myocardial strain hypokinesis (reduced radial, fiber, and cross-fiber strains) was also observed in HCM in the same region, and was found to be correlated with FA. The correlation between FA and hypokinesis was found to be stronger in the cross-fiber direction (part of the passive myocardial function) compared to the fiber direction (part of the active myocardial function). This is consistent with the hypothesis that the principal feature of HCM is the reduction of myocardium passive compliance. The angle between principal shortening and fiber orientation was markedly disordered in HCM, indicating an abnormal transmural coupling.



Conclusion

Myofiber disarray in HCM is correlated with abnormalities of both passive and active myocardial function, and the normal patterns of fiber shortening and wall thickening are deranged in HCM. J. Magn. Reson. Imaging 2006. © 2005 Wiley-Liss, Inc.

https://onlinelibrary.wiley.com/doi/pdf/10.1002/jmri.20473

Imaging myocardial fiber disarray and intramural strain hypokinesis in hypertrophic cardiomyopathy with MRI

We present a method for diffusion tensor MRI in the beating heart that is insensitive to cardiac motion and strain. Using a stimulated echo pulse sequence with two electrocardiogram (ECG) triggers, diffusion-encoding bipolar gradient pulses are applied at identical phases in consecutive cardiac cycles. In this experiment, diffusion is encoded at a single phase in the cardiac cycle of less than 30 ms in duration. This encoding produces no phase shifts for periodic motion and is independent of intervening strains. Studies in a gel phantom with cyclic deformation confirm that by using this sequence we can map the diffusion tensor free of effects of cyclic motion. In normal human subjects, myocardial diffusion eigenvalues measured with the present method showed no significant change between acquisitions encoded at maximum contractile velocity (peak) vs. at myocardial standstill (end-systole), demonstrating motion independence of in vivo diffusion measurements. Diffusion tensor images acquired with the present method agree with registered data acquired with a previous cardiac diffusion MRI method that was shown to be valid in the normal heart, strongly supporting the validity of MRI diffusion measurement in the beating heart. Myocardial sheet and fiber dynamics measured during systole showed that normal human myocardial sheet orientations tilt toward the radial during systole, and fiber orientations tilt toward the longitudinal, in qualitative agreement with previous invasive studies in canines. These results demonstrate the technique's ability to measure myocardial diffusion accurately at any point in the cardiac cycle free of measurable motion effect, as if the heart were frozen at the point of acquisition.

https://onlinelibrary.wiley.com/doi/pdf/10.1002/mrm.10188

Cardiac diffusion MRI without motion effects.

The mechanism of ventricular thickening in normal humans was investigated using in vivo MRI. The hypothesis that myocardial laminar sheets contribute to ventricular thickening predominantly via sheet shear and sheet extension, as previously found invasively in canine studies at particular ventricular sites, was tested. In normal human subjects, registered images of myocardial sheet architecture and strain at the mid-left ventricle (mid-LV) at mid-systole were acquired with diffusion and strain MRI. Sheet function was analyzed by computing myocardial strain in the local fiber-sheet coordinates. In general, myocardial sheets contribute to ventricular thickening through all three cross-fiber strain components: sheet shear, sheet extension, and sheet-normal thickening (previously undocumented). Each of these components demonstrated substantial spatial heterogeneity, with sheet shear and sheet extension usually predominant in the anterior free wall, and sheet-normal thickening predominant near the right ventricular (RV) insertions. However, considerable intersubject variability was also found. In all cases, the contributions to thickening of fiber strains were small. Sheet function in normal humans was found to be heterogeneous and variable, contrasting with the uniform and symmetric ventricular patterns of fiber shortening and wall thickening. The study demonstrates that noninvasive NMR imaging is a promising tool for investigations of myocardial sheet architecture and function, and is particularly suited to the evident complexity of this field of study.

https://onlinelibrary.wiley.com/doi/pdf/10.1002/mrm.10482

Combined diffusion and strain MRI reveals structure and function of human myocardial laminar sheets in vivo.

Quantitative measurements of inherently three-dimensional (3D) cardiac strain and strain rate require 3D data; MRI provides uniquely high sensitivity to material strain by combining phase contrast with single-shot acquisition methods, such as echo-planar imaging (EPI). Previous MRI methods applied to 3D strain used multiple two-dimensional (2D) acquisitions and suffered loss of sensitivity due to magnification within the strain calculation of physiologic noise related to cardiac beat-to-beat variability. In the present work, each single-shot acquisition generates 3D image data by acquiring two contiguous 2D Fourier transform (FT) images in a single echo train of an EPI readout. Although strain encoding divides across multiple EPI shots, each strain component is computed only within single-shot data, avoiding noise magnification. Strain tensor maps are displayed using iconic 3D graphics or a simple color code of tensor shape. In a deforming gel phantom, gradient-recalled echo (GRE) MRI movies of 3D strain rates match expected strain fields. In normal human subjects, 3D strain rate tensor movies of heart and brain comprising seven slices in each of seven cardiac phases were completed in 56 heartbeats. Stimulated echo (STE) MRI of net systolic 3D strain was also demonstrated. Two-slices-in-one-shot spatial encoding permits a complete quantitative survey of ventricular 3D strain in under a minute, with routine patient supervision and turnkey image processing.

Jiangang Dou

Papers

Imaging myocardial fiber disarray and intramural strain hypokinesis in hypertrophic cardiomyopathy with MRI

Cardiac diffusion MRI without motion effects.

Combined diffusion and strain MRI reveals structure and function of human myocardial laminar sheets in vivo.

Phase contrast MRI of myocardial 3D strain by encoding contiguous slices in a single shot