Carlos Milovic1, Christian Langkammer2, José Pedro Marques3, and Karin Shmueli1
1Department of Medical Physics and Biomedical Engineering, University College London, London, United Kingdom, 2Department of Neurology, Medical University of Graz, Graz, Austria, 3Donders Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, Netherlands
Synopsis
The
2019 QSM Reconstruction Challenge compared how different algorithms
reconstructed QSM from true local field maps. However, this neglects
the importance of residual background fields, and how they degrade
the solutions. Here, we used a realistic “total field”
simulation to compare three different background field removal
methods, and to estimate the susceptibility maps resulting from three
state-of-the-art QSM algorithms. We also compared the performance of two
single-step algorithms, that use the total field map as an input. Our
results showed that the two-step Weak-Harmonic QSM method is robust
against residual fields and achieved the lowest error scores,
outperforming single-step methods.
INTRODUCTION
Quantitative
Susceptibility Mapping (QSM) is increasingly used to study iron
accumulation, calcifications, and demyelination in the brain1,2.
QSM solves an ill-posed inverse problem, called dipole inversion,
where susceptibilities are derived from the (“local”)
magnetization fields generated by the objects in the region of
interest (ROI)3.
This process is prone to artifacts and is affected by pre-processing
steps including phase unwrapping and background field removal (BFR).
Therefore, numerous QSM algorithms have been proposed and were
compared in the 2019 QSM Challenge (RC2)4.
RC2 used realistic simulated noisy local field maps5
to quantify the accuracy of a wide range of dipole inversion
algorithms. Background fields were not included in the simulated
field maps and, therefore, robustness against residual
background fields was not assessed. Here, we present a pilot
study using the simulated SIM2 phantom created for RC2 with
additional background fields. In contrast to a simple brain model
used in a previous comprehensive comparison of BFR algorithms6
(which did not estimate their impact on QSM reconstructions), this
SIM2 model includes a more realistic simulation of sources outside
the ROI, including bone, tissue, and air cavities. We compared three
popular BFR algorithms and evaluated their performance when combined
with three cutting-edge dipole inversion algorithms. As BFR is
implicitly included in “single-step” QSM algorithms7,8,
we also compared the performance of two single-step algorithms, which
use the total field as the input.METHODS
The
toolbox used to simulate the ground truth and multi-echo acquisitions
for RC25
includes a noiseless simulation (SIM2, which also included a strong
calcification) with additional realistic background fields.
We added noise (SNR=100) to the 1mm3
complex
signals at all four TEs and performed a nonlinear multi-echo fit9
to estimate the total field map. To obtain the “true” local field
map, we repeated this procedure on the (SNR=100) multi-echo
simulation used in RC2 that did not include any background fields.
Using the total field map (Figure 1) and the “true” local field
map (Figure 2), we performed the following reconstructions and
comparisons:
1.
BFR comparison. The Projection onto Dipole Fields Method (PDF)10,
Laplacian Boundary Valued (LBV)11,
and Variable Sophisticated Harmonic Artifact Reduction for Phase data
(VSHARP)12
methods were applied to the total field map, using the supplied brain
mask. Results were compared in terms of the Root-Mean-Squared-Error
(RMSE) against the “true” local field map.
2.
“Gold standard” QSM reconstructions were generated from the
“true” local field map. We used Fast Nonlinear Susceptibility
Inversion (FANSI13,
winner of the RMSE category RC2, Stage 2) and Nonlinear Dipole
Inversion (NDI14,
a fast, non-regularized solver, reported to be robust against
residual background fields) algorithms.
3.
QSM reconstructions on the local field maps from 1.: We applied
FANSI, NDI, and Weak Harmonic QSM (WH-QSM15,
an extension to FANSI that incorporates joint estimation of residual
background fields and dipole inversion).
4.
Single-step reconstructions: We used the linear WH-QSM model with the
total field as the input, without initialization or preconditioning.
In
addition, we used the GrazTGV single-step toolbox8.
This algorithm inverts a wave-like operator instead of the dipole
kernel and uses the Laplacian of the total field as the input. To
prevent boundary-condition-related artifacts, the ROI mask (evaluation mask) was eroded
by 3
voxels.
QSM reconstructions were optimized to minimize RMSE inside
the RC2 evaluation mask. We also compared the Susceptibility-optimized Similarity Index Metric (XSIM)16
for all optimized reconstructions.RESULTS
BFR
results are shown in Figure 2, with PDF achieving the lowest errors
in both the brain and evaluation masks. Gold-standard
reconstructions, two-step, and single-step results are shown in Figure
3 (only optimal reconstructions using PDF BFR are shown). Two-step
WH-QSM achieved the lowest RMSE and largest XSIM, for all methods,
followed closely by the single-step WH-QSM. Two-step WH-QSM also
showed the least variance across different local field inputs (more
consistent results), and the harmonic phase residual estimates that
it removes closely resemble the BFR error maps near the boundaries
(Figure 4), demonstrating its efficiency in removing residual
background fields.DISCUSSION
While
VSHARP achieved lower errors than LBV in estimating the local field
map, VSHARP’s error map reveals structural errors not present in
other methods. VSHARP may suppress real local fields, and therefore
result in worse QSM reconstructions. This is also suggested by
WH-QSM’s harmonic phase estimation, which shows lower amplitude
residuals for VSHARP than for other methods, and a lower visual
correlation with the VSHARP error map. Single-step algorithms
achieved competitive results, although Laplacian-based methods
(GrazTGV) are prone to artifacts, have poorer noise management, and
may also result in tissue susceptibility underestimation.CONCLUSION
In
this pilot study, we found that WH-QSM is robust in removing residual
background fields, regardless of the prior BFR method. For this
phantom, PDF yielded the lowest errors for all dipole inversion
algorithms. In its linear formulation, WH-QSM produced single-step
reconstructions with errors comparable to using two-step WH-QSM after
PDF BFR. Single-step WH-QSM outperformed the GrazTGV method. We
tested the use of a simulated total field map to test BFR and
single-step algorithms and evaluate the interaction between BFR
methods and dipole inversion methods. This interaction is crucial for deploying
QSM pipelines and could be a possible element of future QSM
Reconstruction Challenges (3.0).Acknowledgements
We
thank Cancer
Research UK Multidisciplinary Award C53545/A24348 for its funding
support. Karin Shmueli is supported by European Research Council Consolidator Grant DiSCo MRI SFN 770939References
1.
Ravanfar P, Loi SM, Syeda WT, Van Rheenen TE, Bush AI, Desmond P,
Cropley VL, Lane DJR, Opazo CM, Moffat BA, Velakoulis D, Pantelis C.
Systematic Review: Quantitative Susceptibility Mapping (QSM) of Brain
Iron Profile in Neurodegenerative Diseases. Front Neurosci. 2021;15. doi:10.3389/fnins.2021.618435
2.
Acosta-Cabronero J, Betts MJ, Cardenas-Blanco A, Yang S, Nestor PJ.
In Vivo MRI Mapping of Brain Iron Deposition across the Adult
Lifespan. J. Neurosci. 2016;36:364–374 doi:
10.1523/JNEUROSCI.1907-15.2016.
3.
Shmueli K. Chapter 31 - Quantitative Susceptibility Mapping. Advances
in Magnetic Resonance Technology and Applications, Academic Press,
2020(1):819-838. doi:10.1016/B978-0-12-817057-1.00033-0
4.
QSM Challenge Committee: Bilgic B, Langkammer C, Marques JP, Meineke
J, Milovic C, Schweser F. QSM Reconstruction Challenge 2.0: Design
and Report of Results. Magn Reson Med. 2021;86:1241-1255
doi:10.1002/MRM.28754 *all authors contributed equally
5.
Marques JP, Meineke J, Milovic C, Bilgic B, Chan K-S, Hedouin R, van
der Zwaag W, Langkammer C, and Schweser F. QSM Reconstruction
Challenge 2.0: A Realistic in silico Head Phantom for MRI data
simulation and evaluation of susceptibility mapping procedures. Magn
Reson Med. 2021;86: 526– 542 doi:10.1002/mrm.28716
6.
Schweser, F., Robinson, S. D., de Rochefort, L., Li, W., and Bredies,
K. (2017) An illustrated comparison of processing methods for phase
MRI and QSM: removal of background field contributions from sources
outside the region of interest. NMR Biomed., 30: e3604. doi:
10.1002/nbm.3604.
7.
Chatnuntawech I, McDaniel P, Cauley SF, Gagoski BA, Langkammer C,
Martin A, Grant PE, Wald LL, Setsompop K, Adalsteinsson E, Bilgic B.
Single-step quantitative susceptibility mapping with variational
penalties. NMR Biomed. 2017;30:e3570. doi:10.1002/nbm.3570
8.
Langkammer C, Bredies K, Poser B, Barth M, Reishofer G, Fan AP,
Bilgic B, Fazekas F, Mainero C, Ropele S. Fast quantitative
susceptibility mapping using 3D EPI and total generalized variation.
Neuroimage 2015;111:622-630.
9.
Liu T, Wisnieff C, Lou M, Chen W, Spincemaille P, Wang Y. Nonlinear
formulation of the magnetic field to source relationship for robust
quantitative susceptibility mapping. Magn Reson Med. 2013;69:467-476.
doi:10.1002/mrm.24272
10.
Liu T, Khalidov I, de Rochefort L, Spincemaille P, Liu J, Tsiouris
AJ, Wang Y. A novel background field removal method for MRI using
projection onto dipole fields (PDF). NMR Biomed. 2011;24:1129-36.
11.
Zhou D, Liu T, Spincemaille P, Wang Y. Background field removal by
solving the Laplacian boundary value problem. NMR Biomed.
2014;27:312-319. doi:10.1002/nbm.3064
12.
Li W, Wu B, Liu C. Quantitative susceptibility mapping of human brain
reflects spatial variation in tissue composition. NeuroImage 2011;
55(4): 1645–1656.
13.
Milovic C, Bilgic B, Zhao B, Acosta-Cabronero J, Tejos C. Fast
nonlinear susceptibility inversion with variational regularization.
Magn Reson Med. 2018;80:814-821. doi:10.1002/mrm.27073
14.
Polak, D, Chatnuntawech, I, Yoon, J, et al. Nonlinear dipole
inversion (NDI) enables robust quantitative susceptibility mapping
(QSM). NMR Biomed. 2020;e4271. doi:10.1002/nbm.4271
15.
Milovic C, Bilgic B, Zhao B, Langkammer C, Tejos C, Acosta-Cabronero
J. Weak-harmonic regularization for quantitative susceptibility
mapping. Magn Reson Med. 2019;81:1399-1411.
16.
Milovic C, Tejos C, and Irarrazaval P. Structural Similarity Index
Metric setup for QSM applications (XSIM). 5th International Workshop
on MRI Phase Contrast & Quantitative Susceptibility Mapping,
Seoul, Korea, 2019.
17.
Milovic
C
and
Shmueli K. Automatic, Non-Regularized Nonlinear Dipole Inversion for
Fast and Robust Quantitative Susceptibility Mapping. 29th
International Conference of the ISMRM, 2021:p3982.