Displacement Field Fitting for Calculating 3D Myocardial Deformations from Tagged MR Images


Walter G. O'Dell, Christopher C. Moore, William C. Hunter,
Elias A. Zerhouni, and Elliot R. McVeigh

The Departments of Biomedical Engineering and Radiology
JHU Medical Imaging Lab
Johns Hopkins University School of Medicine
Baltimore, Maryland, 21205

Abstract

Purpose: Our goal was to reconstruct three-dimensional (3D) myocardial deformation from orthogonal sets of parallel-tagged MR images.
Materials and Methods: Displacement information in the direction normal to the undeformed tag planes was obtained from points along tag lines. Three independent sets of 1D displacement data were used to fit for an analytical series expression describing 3D displacement versus deformed position. The technique was demonstrated on computer-generated models of the deforming left ventricle and on data from normal human volunteers.
Results: Model deformations were reconstructed with 3D tracking error of less than 0.3 mm. Error between estimated and observed 1D displacements along the tags for ten human subjects averaged 0.0+/-0.36 mm. Robustness to uncertainty in the data was demonstrated using a Monte Carlo simulation.
Conclusion: The combination of rapidly acquired parallel-tagged MR images and field-fitting analysis is a viable tool for high resolution cardiac mechanics research and for the clinical assessment of cardiac mechanical function.

Introduction

The techniques of MRI tagging [Zerhouni88, Axel89, Mosher90, Bolster90, Young92, ODell94gr, Fischer93] and fast, breath-hold imaging [McVeigh92, Atkinson91] are promising tools for studying the function of the heart wall non-invasively in both research and clinical settings. The objective of this research is to measure non-invasively the time evolution of the (3D) deformation field within the heart wall. Myocardial tags are regions where the magnetization has been perturbed prior to imaging and therefore produce a signal difference compared to non-tagged regions for a time proportional to T1. Since the tags result from perturbations of the magnetization of the tissue itself, the deformation of the tags accurately reflects the motion of the underlying tissue [Moore94, McVeigh91, Young93]. Special techniques are needed to reconstruct the 3D motion of the heart from MR image planes that are fixed in space, since different sections of tissue are sampled at different times. The movement of the heart through short axis image planes, known as cardiac through-plane motion, is typically ~10 mm at the base of the left ventricle [Rogers91] [This was also validated with an analysis of the ten normal human subjects presented in this paper.] Correcting for this is crucial even for 2D analysis of wall deformation [Moore92]. This correction was achieved by combining information from both long and short axis sets of tagged heart images into a unified expression for the 3D displacement field.

Previously presented material point tracking schemes for MRI tag data require identifiable points within the images, such as intersections between tags [Axel89improved, McVeigh91] , between tags and myocardial contours [Moore92] , or points along striped tag lines [Moore93SMRI]. However, analyses based on such sparse tag intersection data neglect valuable information contained in the intervening portions of the tag lines. Accordingly, the resulting descriptions of deformation suffer from poor spatial resolution. Intersection methods also require images with high spatial resolution both in the frequency and phase directions, leading to acquisition times longer than one breath-hold and thus limiting their clinical applicability.

In this paper we present a novel method for reconstructing the 3D deformation field of the left ventricle (LV) from tagged MR images which uses position and displacement information along the entire length of each tag and relies on accurately defined tag profiles [Atalar94] rather than poorly defined heart contours [Bazille94] . This approach eliminates the need for accurate simultaneous measurement of displacement in two dimensions and permits the computation of the 3D deformation gradient tensor at any point in the heart wall.

To test the performance of the method, a computer-generated model of a prolate spheroid undergoing deformations simulating those measured in the beating heart were analyzed. Finally, the method was applied to parallel tagged, breath-hold cine data sets from ten human hearts. Noise propagation properties using a Monte Carlo analysis were then tested using human cardiac geometry and deformation.

Methods

Parallel-Tagged Data Sets

A typical 3D tag data set of an in vivo human heart consisted of three sets of multiphasic images: one in the cardiac long axis view and two in the cardiac short axis view. To maximize the sampling symmetry and density, the short axis image sets were prescribed as stacks of six or seven contiguous parallel slices while the long axis image set consisted of six slices prescribed radially around the cardiac long axis with an angular separation of 30 degrees. For each image set, a stack of parallel tag planes oriented perpendicular to the readout direction was obtained at eight to twelve time frames throughout systole. The three sets of tag planes corresponded to three orthogonal Cartesian coordinate axes. Portions of a representative human image set are shown in Figure 1.

Fig. 1 Images of an in vivo human heart from a normal volunteer using the conventional tagging and imaging protocol. The progression (from left to right) through three phases in the cardiac cycle are shown: early, mid, and late systole. Two cardiac short axis and one long axis image are shown, each displaying tag lines from a different set of mutually orthogonal tag planes.

The images were then processed by a semi-automated software package [Guttman94] to define positions along the tag lines and around the endocardial and epicardial heart contours. A typical tag and contour data set for a normal human after image processing is shown in Figure 2.


Fig. 2 Left: A typical 3D tag data set for x-displacement in an in vivo human heart from a normal volunteer, showing the appearance of the tags and the contours near end-systole on 7 short axis image planes. Right: A typical 3D contour data set and the estimated prolate spheroidal centroid (upper grey circle) and apical focal point (lower black circle).

For a tag separation in the reference state of 6.0 mm, approximately twelve tags were produced in the myocardium in each set. At a point separation along each tag of 1 mm, this gave over 4600 raw data points, of which every other point was used for the fitting.

Field Fitting

In general terms, field-fitting is a technique for estimating the value of some parameter throughout a particular region of interest, given discrete samples of that parameter in and around that region. In displacement field-fitting, the parameter of interest is the 3D displacement vector and the samples are the values of 1D displacement measured at points on tags in the heart wall. Although field-fitting is generally applicable to any motion detection method, it has been applied here to the analysis of three independent 1D sets of displacement measurements from parallel tagged MR images. This type of data is depicted in Figure 3, which diagrams a short axis image and a deformed set of tags.

Fig. 3 Depiction of a short image at some time after initial tagging. The inset depicts an enlarged view of one deformed tag line after detection of tag points at 1 mm intervals.

Fig. 4 Deformation of a tag plane into a tag surface in 3D. The bold curves are the intersections of the tag surface within the heart wall with four vertical image planes. The enlarged dots on these curves are the tag points generated by an automated tag detection algorithm. xn represents the 1D displacement associated with the nth tag point. The rectangle in the figure at the upper left shows the region of the heart depicted in the lower figure.

The key concept of the method is shown in Figure 4. In three dimensions, each observed tag line represents the intersection of a deformed tag surface with the 2D image plane. The tag surface results from the deformation of an initially flat tag plane. The figure depicts a tag surface within the heart wall that is cut by four parallel image planes. In each plane, tag points were marked along tag lines between the endocardial and epicardial heart contours. For each tag point on the deformed tag surface, the component of its displacement vector that was normal to the tag plane (x in Figure 4) and its position were measured. Reconstruction of the displacement field was performed using the tag point displacement and position data to solve for the coefficients of a series expression describing the field. This is analogous to using digital sampling and Fourier analysis to reconstruct a continuous 1D signal. Here, this expression described the displacement over the entire LV. In the simplest case, each unidirectional displacement data set was used to solve for an interpolation function for the displacement field in that one direction, independent of the motion in the other Cartesian directions. Once the three independent displacement field expressions were determined, they could then be used to compute the 3D displacement of any point in the deformed heart wall. At higher complexity, displacement data from multiple directions can be used simultaneously to solve for the full displacement vector field in an any coordinate system. The displacement field at each time frame was computed independently, using the time at which the tag planes were generated as the universal reference state.

Fitting to a Cartesian Power Series

As an initial step, a first order power series expansion in x, y, and z was used to remove the large scale bulk motions and linear stretches and shears. This greatly increased the efficiency of the prolate spheroidal fitting by aligning the fixed centroid and long axis of the prolate spheroidal coordinate system over time. In addition, large bulk deformations may cause the centroid or apical focus to intersect the myocardium creating a mathematical singularity within the heart wall; the Cartesian fit eliminates this problem. The expression for the displacement in x, x(x,y,z) (refer to Figure 4), took the form:

x = a0 + a1x + a2y + a3z

In vector notation this can be written [in this paper vectors are denoted with a lower case bold italic font, tensors are upper case bold italic, and scalars are plain italic.]

x = a p

where a = [a0,a1,a2,a3] and p = [1,x,y,z]. For each sampled tag point (xn,yn,zn), each term in the vector p was evaluated and the x displacement value, xn, measured. By considering the x-displacements and p vectors of all tag points, a series of simultaneous equations was created and the unknown coefficients (a) were fit using singular value decomposition (a least-squares fitting method) [Press88]. Series expressions for the y and z displacement fields were generated and fit analogously.

Fitting to a Prolate Spheroidal Series

To efficiently describe the curvilinear deformations expected in the heart, the first order Cartesian fit was followed by a prolate spheroidal fit of the residual displacement fields.

Fig. 5 The prolate spheroidal coordinate system. Surfaces of constant are ellipsoids and surfaces of constant longitudinal coordinate, , are hyperboloids.

Figure 5 shows the prolate spheroidal coordinate system where is the radial component, is the longitudinal angle, is the circumferential angle, and f is the focal length. These are related to Cartesian coordinates via

x = f sinh() sin() cos()
y = f sinh() sin() sin()
z = f cosh() cos()

For each prolate spheroidal coordinate displacement field, a series expansion in prolate spheroidal coordinates (, , ) was created using a generating function that is analogous to the spherical harmonic series:

where Pl m is the associated Legendre polynomial function, and the unknown coefficients, ai, were numbered sequentially. For the typical tagging and imaging geometry, and typical image signal-to-noise characteristics, we found that a fit using N=1, L=4 (where N is the radial fitting order and L is the angular fitting order) was most appropriate [ODell94ffSMR], generating 50 free fitting parameters per coordinate direction.

To fit for the coefficients of the prolate spheroidal series expansions from measures of displacement in the Cartesian coordinate directions, the measured displacements were projected onto the local prolate spheroidal axes. The infinitesimal displacements in Cartesian and prolate spheroidal coordinates are related by the following directional derivatives:

where x = [x, y, z], =[, , ] c and the J is the Jacobian matrix for the this coordinate transformation. For a, b, and c defined as the vectors of unknown coefficients for the , , and expressions, respectively, and p the vector of 50 series terms derived from the generating function, then = a*p, = b*p, and = c*p. For the case where the Cartesian axes (as defined by the three orthogonal sets of tag normals) are centered and aligned with the prolate spheroidal coordinate system as described in equations 1-3, the measured Cartesian displacements can be expressed:

where now = [a0,...,a49, b0,...,b49, c0,...,c49], x = [ J00 p0, ... , J00 p49, J01p0, ... , J01p49, J02p0, ... , J02p49 ]. y and z were defined analogously. Similar to the method of solution of the Cartesian power series coefficients above, each measured displacement value was collected into a single row vector, x, and the corresponding vectors were inserted as columns in a matrix P. The unknown coefficients , were then solved using the equation

x = * P

In this way, all the unknown coefficients can be solved simultaneously using all the available tag data and singular value decomposition. Although for finite deformations the relations between the displacements in x, y, and z and those in , , and are not exact, the simultaneous least-squares fitting will always find the optimal fit of the given displacement data to the series expansion.

The fitting procedure was performed independently for each time frame in the data set. Since the heart geometry changes throughout the cardiac cycle, a new prolate spheroidal coordinate system was calculated for every time frame based upon the measured epicardial contour point data. This was done by first estimating the 3 coordinates of the centroid and the 3 coordinates of the apical focus (point on the long axis, toward the apex, at a distance of a focal length from the centroid) and computing a least-squares optimal value at this centroid and apical focus for the given set of epicardial LV contour points. Within an iteration loop, the 6 coordinates were then independently adjusted until the combination of centroid and focal point coordinates and radial coordinate, , was found that produced a prolate spheroid with the smallest fitting error to the measured LV contour points.

Variation of the prolate spheroidal coordinate centroid and apical focus required a modification to Equation 6 to account for the coordinate transformation necessary to align the axes of the new spheroidal coordinate system with that defined by the normals to the undeformed tag planes. For the transformation to the new coordinate system (x') defined by the rotation matrix R, such that x' = R * x, Equation 4 becomes:

x = R-1 * J *

and this modification was carried through the derivation. In addition, this formalism permits 3D reconstruction from sets of images with arbitrary tag normals, so long as three dimensions are spanned.

Computing Strains at Material Points

A material point is defined as a physical piece of myocardial tissue. The mechanical state at a material point in the heart at any given imaging time is fully described by its deformation gradient tensor, F [Malvern69] via: dx = FdX, where x are the coordinates of the point in the deformed state and X are its coordinates in the reference state. F was calculated from the displacement gradient tensor, u, which was computed numerically by taking partial derivatives of the displacement expressions with respect to the three coordinate directions. Because the terms in the series expansion were computed based on the coordinates of the tag points in their deformed state, u described the motion from the deformed state back to the undeformed state. Thus, to compute F from u required an inverse operation: F = (I - u)-1, where I is the identity tensor. The Lagrangian finite strain tensor, E, can then be computed from E = 1/2 (FT F - I) where the `T' superscript denotes matrix transpose.

For both the mathematical and experimental models, a set of material points was defined within the heart wall in the first time frame and 3D displacements and deformations were evaluated over time at these points as they moved through space. A mesh of 96 material points regularly spaced in , , and was selected, based on the imaging and heart geometries. The material point locations at the first time frame were constrained longitudinally by the most basal and most apical short axis image slices and radially by the endocardial and epicardial contours. The interpolation of the contour boundaries between image slice locations was achieved by fitting the LV epicardial and endocardial contour points of the first time frame to a 4th order prolate spheroidal coordinate expansion for as a function of the two angular coordinates.

Analytical Test Case

To test the performance of the method on a known deformation field, a realistic, computer-generated deformation model was constructed. We adapted to prolate spheroidal coordinates an axisymmetrically deforming cylinder model described by Young and Axel [Young92] based on 3D strains measured from cine-radiography of implanted metallic beads in the LV free wall [McCulloch91] . The governing equations describing the deformed coordinates (,, ) as a function of the initial coordinates (,, ) and the deformation parameters, were as follows: where f is the focal length of the prolate spheroidal coordinate system and Vol() is the volume within a prolate spheroidal shell of constant . Deformation in the radial component, , was limited to a volume conserving (incompressible) contraction mode by setting = 1. The initial and deformed short axis endocardial equatorial radii, f*sinh(endo) and f*sinh(endo), were chosen to approximate realistic heart geometry and resulted in an ejection fraction of ~50 percent. The prolate spheroidal deformation parameters are given in Table 1.


Table 1 Axisymmetric deformation model parameters on a prolate spheroid.


Table 2 Cartesian deformation parameters.

Bulk motions and linear deformations incorporating ellipticalization and shears in x, y, and z were then superimposed upon the axisymmetric modes in the manner of Arts, et al. [Arts92]. The magnitudes of these additional modes were chosen to give the overall model approximately physiological rigid body motions and to reproduce those deformations observed by Arts, et al. These deformation values are given in Table 2. Image prescription error, where the central axis of the imaging volume is not coincident with the long axis of the left ventricle, was also simulated with representative values of 5 degrees offset about the X axis and 8 degree about the Y axis.

Seven image slices and ten tag planes were simulated for each each image set. Separation between adjacent data points along a given tag was fixed at 2 mm. Over the entire 3D data set, this produced approximately 2400 tag data points. The prolate spheroid deformation model is shown in Figure 6. The two short axis image sets are spatially coincident, giving a grid tag appearance.

    Fig. 6 Simulated short axis (Left) and long axis tag data sets for the prolate spheroid model. Physiologic deformation modes with added Cartesian motions were modeled for 7 image slices and 10 tag planes in each view. The angles of tilt are due to simulated image prescription error.

Human Data Sets

Ten normal human volunteers were imaged on a 1.5 Tesla scanner using a cine breath-hold imaging sequence with parallel tags [McVeigh92], after giving informed consent. Each of the 18 acquisitions in each subject was performed during a breath-hold. Volunteers were scanned at end expiration in the supine position using a flexible surface coil wrapped around the left side of the chest. The imaging parameters for each slice were: TR=7.0ms, TE=2.3ms (fractional echo), 15 degree flip angle, 110 phase encoding steps, 1.25 x 2.9 x 7mm voxels, one average, 5 phase encode views per movie frame (35ms time resolution). The tagging pulse consisted of 5 non-selective rf pulses with relative amplitudes of 0.7, 0.9, 1.0, 0.9, 0.7 separated by SPAMM [Axel89] encoding gradients to achieve a tag spacing of 6mm. The tagging tip angle was tuned to achieve a 180 degree flip angle.

Monte Carlo Simulations

A representative human data set was fit and the reconstructed deformation field and heart geometry was then used to generate a noise-free parallel tag data set. The effect of uncertainty in tag point position on the final material point tracking predictions was evaluated using a Monte Carlo simulation [Press88] on the reconstructed data set. One-dimensional Gaussian noise profiles of 0.25 to 1.0 mm standard deviation were added to the x, y, and z data sets, and the resulting 3D material point trajectories were computed for the 96 material points over 100 trials. A single root-mean-square deviation (RMSD) value was computed for each point from the 3D distribution of the cloud of estimated point trajectories around the expected location.

Results

Two measures of the displacement field-fitting performance were evaluated with the prolate spheroid deformation model: tracking and fitting. The 3D tracking performance was evaluated by comparing the estimated material point trajectories derived from the field-fitting reconstruction to the exact solution computed from the deformation model Equations 6-8. The mean absolute value and the standard deviation of the tracking error were computed for the set of 96 material points. The fitting performance was evaluated by computing the standard deviation of the error (SDE) (around a mean error of zero) between the estimated and the measured 1D displacements at each tag point. Thus, the fitting performance reflects the ability of the reconstruction to account for the variations in the displacement field at the locations where the measurements were made, while the tracking performance reflects both the quality of the fitting and the interpolation of the displacement field between the measurement locations.

Mathematical Deformation Model Results

The SDE of the fit to the ~2400 model tag data points was 0.095 mm. This is below the expected uncertainty in the determination of tag point displacements for typical in vivo data sets [Atalar94]. This implies that the fitting error for a human data set will be dominated by the uncertainty in the tag point displacement data rather than error in reconstructing the displacement field at the measurement locations. The 3D tracking errors over the set of 96 material points was 0.28 +/- 0.16 mm (mean +/- SD). The relatively large value of the 3D tracking error (~0.3mm) compared to the SDE of the fit (~0.1mm) suggests that further improvements to the reconstruction can be made by increasing the tag density and number of fitting parameters. The corresponding circumferential strain errors at the 96 material points were 0.006 +/- 0.012 for a range of -0.25 to 0.06, the longitudinal strain errors were 0.0003 +/- 0.007 over the range -0.23 to -0.08, and the midwall radial strain errors were 0.017 +/- 0.026 for a range of midwall radial strains of 0.18 to 0.52. The accuracy of the strain estimations, even where 3D tracking errors were ~0.3mm, results from the correlation of tracking errors between neighboring myocardial regions. These errors and standard deviations are well below the threshold necessary to detect motion abnormalities in the ischemic heart wall[Lugo94].

In Vivo Human Heart Results

The SDE of the fit (about a mean error of zero) to the tag data at 228 ms after the electrocardiograph R-wave was 0.36 +/- 0.06mm (mean SDE +/- SD SDE) for the ten subjects. This number reflects both the error in reconstructing the displacement field, as seen in the fitting results for the mathematical model, and the uncertainty in the determination of the tag point locations. The accuracy of the fitting can be illustrated by the ability to reconstruct the positions of deformed tags. The fitted 3D displacement field was used to generate points that started from the reference state tag plane locations and moved into the image plane at 228 ms into systole.


Fig. 7 Short and long axis images of a human heart at 228ms into systole, overlaid with tag point locations predicted from the 3D field-fit.

Figure 7 shows representative short and long axis human cardiac images 228 ms into systole and demonstrates the agreement between the predicted locations of the tag points and the actual tags in the MR images.

Monte Carlo Noise Analysis

The precision of the fitting algorithm was tested using a Monte Carlo simulation as described in Section 3.5. The root-mean-square deviation (RMSD) of the computed material point position as a function of input noise level is shown in Figure 8.

Fig. 8 The root-mean-square deviation (RMSD) of the computed material point position as a function of input noise level on a human heart geometry and deformation field. The distribution of tracked points formed an isotropic cloud around the noise-free reference trajectory. The RMSD of the cloud at the endocardial and epicardial surface points was the same, but of a larger value than at midwall point locations. The error bars correspond to the standard deviation in the RMSD over the 100 Monte Carlo trials.

The scatter of points around the expected value was found to be isotropic. The root-mean-square deviation (RMSD) of the computed material point position increased linearly as a function of input noise level, as shown in Figure 5. The scatter of points around the expected value was found to be isotropic. The RMSD at the endocardial and epicardial material points was found to be equal, and was greater than that found at the midwall. At an input noise standard deviation of 0.5mm, the midwall RMSD tracking error was 0.077 +/- 0.015 and that at the endocardium and epicardium was 0.126 +/- 0.030. The RMSD computation using a subset consisting of 50 trials gave results that were not significantly different, suggesting that 100 trials were sufficient to obtain a stable convergence of the estimate in tracking precision.

Discussion

The combination of parallel-tag MR imaging and displacement field-fitting is an accurate and robust method for reconstructing the 3D deformation field over the entire left ventricle. Because of its reliance on parallel tag data, the displacement field-fitting method is inherently less susceptible than previous MRI reconstruction schemes to tag and contour detection error since only the centerline of any tag need be determined during image analysis. The incorporation of a greater number of points along each tag line increases the sampling density over the heart compared to techniques that use only those points located at intersections between tags or between tags and myocardial contours.

The fitting of displacement fields can also be realized using other methods, including energy minimization techniques [Young92, Denx94WNAM]. In this approach, the fits can be computed numerically for a predefined set of material points (nodes) and interpolation between these points accomplished via linear or finite element interpolation functions. Although field-fitting by solving for series coefficients has some mathematical similarities to energy minimization and other methods, the series method has several advantages. First, it is independent of material strain energy models. Second, the global fit provides the ability to express the 3D deformation at any myocardial point with a relatively small number of parameters, independent of a predefined set of material points.

The field-fitting approach is immediately suitable to other methods of 3D strain analysis where motions in multiple directions are independently measured. For example, three sets of velocity encoded images [Pelc91] could be used to solve for a set of expressions describing the velocity field over a prescribed region of interest, in a manner analogous to that described for tag-based displacement fields. This would have the advantage of smoothly interpolating the velocity field between pixels and of filtering out uncertainty in the velocity measurements at each pixel. Grid tag data sets can also be analyzed by interpreting the grid as two independent sets of parallel tags.

Conclusions

We have demonstrated the application of displacement field-fitting using an analytical series expression for the analysis of tagged MRI cardiac data. The important features of this method are that it considers all the available tag data, not just points at tag-tag or tag-contour intersections; it allows the determination of the local 3D deformation gradient tensor at any point in the heart wall; it is robust to the expected uncertainty in the displacement data; and it is suitable for the analysis of both grid and parallel tagged MR data. This last property is important in light of recent advances in cardiac breath-hold imaging, virtually free of motion artifact, where only parallel tags are produced. The cascade of a 1st order Cartesian basis set fit and a geometrically more appropriate prolate spheroidal fit enables the reconstruction of material point trajectories to within 0.3 mm for a physiologic deformation model. At late systole in ten normal human subjects, tag displacement data was reconstructed with an average error of 0.00 +/- 0.36mm, where the standard deviation of the error matches approximately the expected uncertainty in the determination of the in vivo tag point displacements. This suggests that all the displacement information contained in the tag data has been accounted for in the reconstruction. The combination of rapidly acquired parallel-tagged MR images and field-fitting analysis is a valuable tool for high resolution cardiac mechanics research and for the clinical assessment of cardiac mechanical function.

Acknowledgements

The authors gratefully acknowledge Dr. Andrew Douglas for thoughtful discussions and Dr. Carlos Lugo-Olivieri for assistance in acquiring the human heart data.