Guido Buonincontri1,2, Jan W Kurzawski2,3, Joshua Kaggie4, Tomasz Matys4, Ferdia Gallagher4, Matteo Cencini2,5, Graziella Donatelli2,6, Paolo Cecchi6, Mirco Cosottini2,6,7, Nicola Martini8, Francesca Frijia9, Domenico Montanaro9, Pedro A Gómez2,10, Rolf F Schulte11, Alessandra Retico3, and Michela Tosetti1,2
1IRCCS Stella Maris, Pisa, Italy, 2Imago7 Foundation, Pisa, Italy, 3Istituto Nazionale di Fisica Nucleare, Pisa, Italy, 4Department of Radiology, University of Cambridge, Cambridge, United Kingdom, 5University of Pisa, Department of Physics, Pisa, Italy, 6U.O. Neuroradiologia, Azienda Ospedaliera Universitaria Pisana (AOUP), Pisa, Italy, 7University of Pisa, Department of Translational Research and New Technologies in Medicine and Surgery, Pisa, Italy, 8Fondazione Toscana Gabriele Monasterio, Pisa, Italy, 9U.O.C. Risonanza Magnetica Specialistica e Neuroradiologia, Fondazione CNR/Regione Toscana G. Monasterio, Pisa, Italy, 10Technical University of Munich, Munich, Germany, 11GE Healthcare, Munich, Germany
Synopsis
Three-dimensional magnetic resonance
fingerprinting with spiral projection k-space
trajectory offers fully-quantitative estimations at a high spatial resolution.
To assess the repeatability and reproducibility of the estimations, we acquired
test/re-test data in the human brain at 1.5T and 3.0T in a travelling head
study involving a total of 12 subjects and 8 different MR scanners. Our
approach estimated
voxel-wise performance in the CNS: variability was assessed using
coefficients-of-variation, bias using a GLM analysis. Solid matter repeatability CVs were under
2% for nPD/T1, and 5% for T2, while reproducibility biases were under 10%
in solid matter compartments for T1/T2.
Introduction:
Magnetic
Resonance Fingerprinting (MRF) efficiently samples the transient state of the
MRI signal to extract multi-parametric, fully quantitative maps1. Recent
studies have shown a high repeatability of T1 and T2 values by 2D SSFP MR Fingerprinting2
in the ISMRM/NIST phantom3, as well as in human volunteers4,5.
MR
Fingerprinting has also been extended to three-dimensional acquisitions6,7,8
for improved spatial resolution and diagnostic value, as well as high
repeatability9. In order to assess the repeatability and
reproducibility of 3D SSFP MRF, we acquired test/re-test data in the human
brain at 1.5T and 3.0T in a travelling head study involving a total of 12
subjects and 8 different MR scanners from a single vendor.Methods:
The data were acquired on eight separate systems as shown in Figure 1c,
all from the same vendor (GE Healthcare, Chicago, IL), each operating either at
1.5T or 3.0T and each with different hardware (RF/gradient coils) and software
release. With local ethical approval, human subjects were imaged in two
identical sessions per scanner, each including a 3D steady-state free
precession MRF with spiral projection k-space acquisition8. Subjects
were removed from the scanner between imaging sessions. To allow for a general
linear model (GLM) analysis, each subject was scanned in multiple MR scanners (Figure
2a). The subjects received also a FSPGR scan at 3T at the same spatial
resolution as 3D MRF. The MRF acquisition trajectories used undersampled spiral
projection interleaves (see Figure 1b) with FOV = (225mm)3, matrix = 200x200x200,
sampling bandwidth = ±250kHz, TE/TR = 0.5/11 ms. The scan parameters are shown
in Figure 1. The
spirals were rewound and followed by a spoiler z-gradient achieving 4pi/mm dephasing. The maximum gradient amplitude was 20mT/m and slew rate was 70T/m/s. The
analysis in this work did not apply system-specific gradient delay or
trajectory correction. MRF maps were
obtained by inner-product pattern matching and the MRF dictionary was computed using the extended phase
graphs formalism10, without including B0 or B1 effects in the model.
M0 values were reported self-normalised to the average inside the brain mask (PDn).
Analysis: the
analysis pipeline matched Buonincontri et
al4. The quantitative maps for every test were rigidly co-registered to their respective re-test
using Statistical Parametric Mapping (SPM 12) Toolbox11. After
registration, each subject’s volumetric image was warped to match a custom
DARTEL atlas (made using the 3D
FSPGR). After applying 6mm Gaussian smoothing, coefficients
of variation were calculated between each voxel in test and retest measurements
to measure the associated variability. Values were reported averaged on each tissue
class, using a threshold of 70% probability as a mask per each tissue (Figure
2b). A general linear model was also estimated assessing the biases associated
with each covariate in the experiment including: test, field, subject and site
(Figure 2a).Results:
Sample co-registered MRF images are
shown in Figure 3, showing fully-quantitative
maps with a high anatomical detail and values within literature ranges.
Voxel-wise coefficients of Variation (CV) between test and re-test are shown in
Figure 4, showing solid matter
repeatability CVs under 2% for nPD andT1, and 5% for T2 (with the exception of
site 8 with CV around 8%). Figure 5 shows the biases associated with field
strength and each individual scanner. Biases associated with site were under 10%
for T1 and T2 in solid matter compartments. T1 showed uniform bias, while T2
displayed the bias pattern typical of B1+ effects at 3.0T, where PDn bias
spatial distribution was consistent with the different receiver coil profiles.Discussion:
We
assessed repeatability and reproducibility of 3D MRF at eight separate imaging
systems, which included both 1.5 T and
3.0 T. Importantly, our
assessment was not limited to regions-of-interest, but estimated voxel-wise
performance; variability was assessed using coefficients-of-variation, bias
using a GLM analysis. Reproducibility values were in agreement with a similar analysis
performed on 2D MRF data4, while repeatability values were improved by
approximately a factor of two. This was perhaps due to the smaller registration
errors and partial volumes, as well as higher SNR efficiency. The data here
presented were in line with other quantitative assessments of repeatability
and reproducibility in the literature using other common mapping techniques12,13,14.
Iterative reconstructions, the inclusion of B1+ or B1- in the model, and a full
characterization of the systems (such as gradient delay and trajectory
estimation) may further improve the robustness of these 3D MRF quantifications.
In
conclusion, three-dimensional MRF with spiral projection k-space trajectory
obtains detailed parametric maps with highly repeatable and reproducible nPD,
T1 and T2 values.Acknowledgements
Support from the Italian Ministry of Health and the Tuscany Region under the project “Ricerca Finalizzata”, Grant n. GR-2016-02361693. Funding from the EMPIR Programme 18HLT05 QUIERO Project, co-financed by the Participating States and from the European Union’s Horizon 2020 Research and Innovation Programme.
References
1. Ma D,
Gulani V, Seiberlich N, et al. Magnetic resonance fingerprinting. Nature.
2013;495(7440):187-192.
2.
Y. Jiang, D. Ma, N. Seiberlich, et
al. MR fingerprinting using fast imaging with steady
state precession (FISP) with spiral readout. Magn. Reson.
Med., 74 (2015), pp. 1621-1631
3.
Y. Jiang, D. Ma, K.E. Keenan
et al. Repeatability of magnetic
resonance fingerprinting T1 and T2 estimates assessed using the ISMRM/NIST MRI
system phantom. Magn. Reson. Med., 78 (2017),
pp. 1452-1457
4. Buonincontri G, Biagi L, Retico A, et al. Multi-site repeatability and reproducibility of MR
fingerprinting of the healthy brain at 1.5 and 3.0T. Neuroimage
2019;195:362-372.
5. Korzdorfer G, Kirsch R, Liu K, et al. Reproducibility and
Repeatability of MR Fingerprinting Relaxometry in the Human Brain. Radiology 2019;292(2):429-437.
6. Ma, D. et al. Fast 3D magnetic resonance fingerprinting for a
whole-brain coverage. Magn. Reson.
Med. 79, 2190–2197
(2018).
7.
C. Liao, B. Bilgic, M.K. Manhard
et al. 3D MR fingerprinting with
accelerated stack-of-spirals and hybrid sliding-window and GRAPPA
reconstruction NeuroImage, 162 (2017), pp. 13-22
8. Cao, X. et al. Fast 3D brain MR fingerprinting based on multi-axis
spiral projection trajectory. Magn
Reson Med 82, 289 (2019).
9. Ma D, Jones
SE, Deshmane A, et al. Development of high‐resolution 3D MR fingerprinting
for detection and characterization of epileptic lesions. J
Magn Reson Imaging 2018;1–14.
10.
Weigel, M. Extended phase graphs: Dephasing, RF pulses, and echoes - pure
and simple. J. Magn. Reson. Imaging
(2014). doi:10.1002/jmri.24619
11.
J. Ashburner. SPM: a history. Neuroimage, 62 (2012), pp. 791-800
12.
B.A. Landman, A.J. Huang, A. Gifford
et al. Multi-parametric neuroimaging
reproducibility: a 3-T resource study. Neuroimage, 54 (2011),
pp. 2854-2866
13.
C.M. Bauer, H. Jara, R. Killiany, et
al Whole brain quantitative T2 MRI
across multiple scanners with dual echo FSE: applications to AD, MCI, and normal
aging Neuroimage, 52 (2010), pp. 508-514
14. S.C. Deoni, S.C. Williams, P. Jezzard
et al. Standardized structural magnetic
resonance imaging in multicentre studies using quantitative T1 and T2 imaging
at 1.5 T Neuroimage, 40 (2008), pp. 662-671