Armando Manduca1, Timothy L Rossman2, David S Lake1, Kevin J Glaser3, Arvin Arani3, Shivaram P Arunachalam3, Phillip J Rossman3, Joshua D Trzasko3, Dan Dragomir-Daescu2, Richard L Ehman3, and Philip A Araoz3
1Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, United States, 2Division of Engineering, Mayo Clinic, Rochester, MN, United States, 3Radiology, Mayo Clinic, Rochester, MN, United States
Synopsis
MR elastography is increasingly being applied to
thin or small structures in which wave propagation is dominated by waveguide
effects, which can bias stiffness results with common processing approaches. Finite
element simulations of a realistic cardiac geometry were used to investigate
the importance of waveguide effects, and to study the ability of the curl operator
to remove these effects. The results establish that waveguide effects in a
cardiac geometry can strongly bias stiffness results, but can be correctly
handled by application of the curl operator to the measured displacement field,
followed by true 3D inversion.
Introduction
MR
elastography (MRE) non-invasively measures mechanical material parameters, such
as shear modulus, in soft tissue. In MRE, an external source generates shear
waves in a tissue of interest. A phase contrast based MRI technique then
measures the vibrational displacements as they propagate through the tissue.
Finally, the displacement field is inverted to generate a map of material
properties1-2. MRE has proven clinically useful in the liver3-5,
and is showing promise for clinical applications in the brain6-8; other
possible applications are being explored.
In some applications, thin or
small structures are being investigated (e.g. bladder, small tumors, etc.)
Waveguide or boundary effects dominate wave propagation in such structures as
the ratio of the wavelength to the thinnest dimension falls below unity, and
propagation depends critically on geometry as well as on the underlying
material properties. In particular, cardiac MRE is actively being investigated
by several groups9-13. The myocardium is a thin shell, and at
current MRE driving frequencies, waveguide effects are strongly present. Many
MRE processing approaches can yield biased results if they do not account for
these effects. Applying the curl operator to the displacement field can remove
waveguide effects in principle, leaving only a field that propagates at the
shear wave speed, although at the expense of noise amplification14-15.
The purpose of this work is to investigate the importance of waveguide effects,
and the ability of the curl operator to remove these effects, on MRE inversions
in a realistic cardiac geometry.Methods
Finite element simulations of a realistic
cardiac geometry were performed with ANSYS 16.1. A linear viscoelastic material
was used with a complex shear modulus of G* = 4 + 1i kPa (thought to be close
to diastolic heart stiffness), Poisson’s ratio of 0.49995, and mass density of
1 g/cm3. The 3D realistic cardiac geometry was obtained from a segmented
ECG-gated computed tomography image volume of a patient’s heart [AM1] in diastole. The
models contained ~6 million nodes with ~22 million degrees of freedom at
0.29x0.29x0.2 mm resolution. Harmonic displacement excitation with 0.05 mm
amplitude was applied in either a shear or longitudinal direction to a group of
exterior nodes at the base of the geometry at various frequencies from 60-220
Hz. The nodes on the most superior face of the heart wall geometry were fully
constrained in all degrees of freedom (Fig 1). The shear modulus was calculated
by direct inversion (DI) of the Helmholtz equation on either the displacement
or curled wave field2. Spatial derivatives were taken using a 3x3x3
6-nearest neighbor kernel at a resolution of 0.29 mm.Results
Figs. 2-3 show results for the realistic cardiac geometry at 100 Hz and
140 Hz, with longitudinal driving at the apex. Results without the curl (Fig.
3) are incorrect and show many artifacts. Results with the curl (Fig. 4) are
fairly uniform and report the correct value with 3D inversion. Results with 2D
inversions, while somewhat improved, remain incorrect with numerous artifacts.
Storage and loss moduli results for a sample case (100 Hz, curl) are shown in
Fig. 4, and the values along the profile show accurate recovery of both
parameters. Similar results to those shown occur with shear instead of
longitudinal driving and at other frequencies (not shown), with biases more
severe at lower frequencies.Discussion and Conclusions
Removing
waveguide effects by inverting the curl of the 3D displacement field has only
been validated to a limited degree with simple models and phantoms14-15,
and not in a complex, realistic heart geometry. These results show that substantial
biases can occur in this geometry, but that applying the curl and performing
full 3D inversion allows accurate recovery of the complex shear modulus. This
is the first demonstration that 3D MRE can, in principle, give accurate shear
modulus measurements for a realistic cardiac geometry.
This
study had several limitations. The models assumed a homogeneous object and
isotropic material properties, whereas the myocardium is anisotropic and far
more complex. The models did not include noise, and applying the curl amplifies
noise in the data, which biases DI results towards softer stiffness values. The
models were inverted with an effective pixel resolution of 0.29 mm, which
minimizes discretization effects, but such effects can become important at
realistic MRE resolution. However, these results establish that at a minimum,
taking the curl of the wave field and performing a full 3D inversion are both
necessary (although not sufficient) steps for accurate estimation of shear
modulus in a cardiac geometry.Acknowledgements
This
work was supported in part by grants from the National Institute of Health R01
EB001981 and R01 HL115144.References
1. Muthupillai
R, Lomas DJ, Rossman PJ, Greenleaf
JF, Manduca A, Ehman RL.
Magnetic resonance elastography by direct visualization of propagating acoustic
strain waves. Science 1995;269:1854–1857.
2. Manduca
A, Oliphant TE, Dresner MA, Mahowald JL, Kruse SA, Amromin E, Felmlee JP, Greenleaf
JF, Ehman RL. Magnetic resonance elastography: Non-invasive mapping of tissue elasticity.
Med Img Anal 2001;5:237-254
3. Yin
M, Talwalkar JA, Glaser KJ, et al. Assessment of hepatic fibrosis with magnetic
resonance elastography. Clin Gastroenterol Hepatol 2007;5:1207–1213.
4. Huwart
L, Peeters F, Sinkus R, et al. Liver fibrosis: non-invasive assessment with MR
elastography. NMR Biomed 2006;19:173–179.
5. Yin
M, Glaser KJ, Talwalkar JA, Chen J, Manduca A, Ehman RL. Magnetic resonance
elastography of the liver: Observations from a review of 1,377 exams. Radiology
2016;278:114-124.
6. Streitberger
K-J, Sack I, Krefting D, Pfuller C, Braun J, Friedemann P, Wuerfel J. Brain viscoelasticity
alteration in chronic-progressive multiple sclerosis. PlosONE 2012;7(1):e29888.
7.
Murphy
MC, Huston J, 3rd, Glaser KJ, et al. Preoperative assessment of meningioma
stiffness using magnetic resonance elastography. J Neurosurg.
2013;118(3):643-8.
8. Murphy
MC, Huston J III, Jack CR, Jones DT, Glaser KJ, Senjem ML, Chen J, Manduca A,
Felmlee JP, Ehman RL. Regional brain stiffness changes across the Alzheimer’s
disease spectrum. Neuroimage:Clinical 2016;10:283-290.
9. Kolipaka
A, Aggarwal SR, McGee KP, Anavekar N, Manduca A, Ehman RL, Araoz PA. Magnetic
resonance elastography as a method to estimate myocardial contractility. Journal
of magnetic resonance imaging. JMRI 2012;36(1):120-127.
10. Elgeti T, Knebel F, Hattasch R,
Hamm B, Braun J, Sack I. Shear-wave amplitudes measured with cardiac MR
elastography for diagnosis of diastolic dysfunction. Radiology
2014;271(3):681-687.
11. Elgeti T, Sack I. Magnetic
resonance elastography of the heart. Curr Cardiovasc Imaging Rep 2014;7:9247.
12. Arani A, Glaser KL, Arunachalam
SP, Rossman PJ, Lake DS, Trzasko JD, Manduca A, McGee KP, Ehman RL, Araoz PA.
In vivo, high-frequency three-dimensional cardiac MR elastography: Feasibility
in normal volunteers. MRM 2016;in press, electronic copy available.
13. Wassenaar PA, Eleswarpu CN, Schroeder
SA, Mo X, Raterman BD, White RD, Kolipaka A. Measuring age-dependent myocardial
stiffness across the cardiac cycle using MR elastography: a reproducibility
study. MRM 2016: 75:1586–1593.
14. Sinkus R, Daire J-L, Vilgrain V,
Van Beers BE. Elasticity imaging via MRI: Overcoming the waveguide limit, and
clinical liver results. Cur Med Img Reviews 2012; 8:56-63.
15. Nenadic I, Bernal M,
Brum J, Gennison J-L, Pernot M, Greenleaf JF, Tanter M, Urban MW. Recovering
shear wave velocity in boundary sensitive media with two-dimensional motion
tracking. Proc IUS Ultrasonics Symposium 2014;1093-1096.