Andreea Hertanu1,2, Lucas Soustelle1,2, Arnaud Le Troter1,2, Julie Buron1,2,3, Julie Le Priellec3, Victor N. D. Carvalho1,2,4, Myriam Cayre3, Pascale Durbec3, Gopal Varma5, David C. Alsop5, Olivier M. Girard1,2, and Guillaume Duhamel1,2
1Aix Marseille Univ, CNRS, CRMBM, Marseille, France, 2APHM, Hôpital Universitaire Timone, CEMEREM, Marseille, France, 3Aix Marseille Univ, CNRS, IBDM, Marseille, France, 4Aix Marseille Univ, CNRS, ICR, Marseille, France, 5Division of MR Research, Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, United States
Synopsis
Inhomogeneous
magnetization transfer (ihMT) signal originates from the residual dipolar interactions
and is weighted by the associated dipolar relaxation time T1D. The resulting
signal can be modulated by filtering the contribution of short T1D
components to emphasize the contrast between different structures, or to
enhance the specificity for myelin imaging. In this study, the dependency of
ihMTR to T1D is investigated theoretically for different T1D-filtering
strengths. Experimental WM/GM relative contrasts for the same configurations are
put in perspective with theoretical contrasts resulted from single-T1D
and bi-T1D biophysical model simulations.
Introduction
The ihMT signal depends on the dipolar order relaxation
time (T1D)1 and can be modulated
by filtering the signal of short T1D components2 (e.g. < 1 ms) so
as to increase the contrast between various structures.
Our main objective was
to establish a general understanding of the response of the ihMTR signal to
different filtering strengths. Single- and bi-T1D biophysical models
were used to derive the theoretical ihMT signal as a function of T1D,
for 4 different filters. Experimental White Matter/Grey Matter (WM/GM) relative
contrast measurements were compared with simulated contrasts. This allowed us
to confirm the bi-T1D theoretical model as a suitable model to
describe the increase in WM/GM relative contrast with increasing filtering
strengths.Methods
MRI
experiments were performed on a preclinical 7T Bruker scanner. Sixteen control
mice C57Bl/6J were scanned with a 3D ihMT-RAGE3 sequence
(TR/TE = 2200/2.1 ms, 100x100x750 µm3 resolution) and a protocol
including 4 ihMT configurations with different T1D-filterings (Figure
1): the single-frequency (MT+) saturation is identical for all
filters, whereas for the dual-frequency (MT±) saturation, the Δt switching time between pulses at alternated
frequency was increased (Δt = 0.8 ms; 1.6 ms; 3.2 ms) to strengthen the filtering
toward higher T1D values. Zero T1D-filtering was obtained
using dual-band cosine-modulated (CM) pulses, which allow irradiation at both
positive and negative frequencies simultaneously. The use of this modified-ihMT
approach4 granted an
increase in Δt values while keeping RF pulses parametrization constant across all
configurations.
The
theoretical dependency of ihMTR with respect to T1D was calculated according
to the formula $$$\text{ihMTR} = 2\times\frac{\text{MT}^{+}-\text{MT}^{\pm}}{\text{M}_{0}}$$$, where the magnetization of the distinct compartments
was simulated according to the Bloch-McConnell-Provotorov equations solved in
the matrix formalism5. The biophysical
models associated with the theory of ihMT, encompassing single- or bi-T1D
component(s) are depicted in Figure 2. The single-T1D model was
simulated over a large range of T1D values [10 µs; 20 ms]. The bi-T1D
model was simulated by fixing the long T1D component at 6.0 ms for
WM4 and 5.8 ms for
GM4 and varying the
short T1D components in the [10 µs; 1 ms] range5. The total pool
size ratios for WM and GM were fixed at 10% and 3.5%, respectively6, and were
distributed among the homogeneous (T1D=0) and inhomogeneous (T1D≠0)
compartments. Other MT parameters, such as relaxation and exchange rates were
fixed to values reported in the literature6.Results
Single-T1D
model (Figure 3a, b): The sensitivity threshold (arbitrarily fixed at 2%) was
reached in WM (resp. GM) for higher T1D values as Δt increased. CM
was sensitive to T1Ds > 0.19 ms (resp. 0.49 ms), Δt0.8
to T1Ds > 0.44 ms (resp. 0.75 ms), Δt1.6 to T1Ds
> 0.64 ms (resp. 1.97 ms) and Δt3.2 to T1Ds > 1.30
ms (resp. 2.54 ms). Long T1D components were also attenuated with
increasing Δt. For T1D = 6.0 ms, an attenuation of 6%, 21% and 57%
was observed for Δt0.8, Δt1.6 and Δt3.2
respectively, relative to the non-filtered CM signal.
Bi-T1D
model (Figure 3c, d): By increasing Δt, ihMTR decreases and the threshold beyond which ihMTR
increases considerably with T1D is shifted toward higher T1D
values (e.g., 70 μs for Δt0.8 and 130 μs for Δt3.2).
A differential in ihMTR values between CM and Δt0.8
configurations was obtained for T1Ds in the [100 µs; 1 ms]
range (Figure 4a, b, green curve), whereas outside this range, the two
configurations show a clear tendency for converging ihMTR values. Consequently,
the ihMTR signal built upon the difference between these two configurations
results in a bandpass shape (albeit associated with reduced sensitivity) and
may represent the means to isolate the ihMTR signal of short T1D
components.
Experiments:
Representative slices of the 3D ihMTR images for the four different filters and
the difference images obtained by subtraction between the non-filtered and
filtered configurations are displayed in Figures 3e and 4c along with the
simulated curves to illustrate the obtained contrasts.
Comparison
(Figure 5): Comparison between quantitative theoretical values
and experimental data shows that the single-T1D model overestimates the
WM/GM relative contrast, while the bi-T1D model provides values
compatible with the experimental ones.Discussion
The
single-T1D model provided a general understanding of the ihMT signal
response to T1D and demonstrated the efficacy of increasing
Δt to attenuate/eliminate the signal associated with
short T1D components. The bi-T1D model provided a better
description of the WM/GM relative contrast, particularly for the CM
configuration which was highly overestimated by the single-T1D model,
consistent with a recent publication5 that
demonstrated the existence of at least two T1D components in WM and
GM tissues.
Additionally, the difference between the non-filtered (CM) and the
filtered (Δt0.8) configurations proved to be a viable solution for the
isolation of a small range of short-T1D components [100 µs; 1 ms].
The WM/GM relative contrast for the range of short T1D components
(CM – Δt0.8) was the lowest, whereas the contrast of the most
filtered configuration (Δt3.2) was the highest, emphasizing an
important difference in the distribution of long T1D components between
the two tissues.Conclusion
A
reliable description of the WM/GM relative contrast can be obtained by using a
biophysical model which includes at least two distinct T1D
components.Acknowledgements
This work was performed by a
laboratory member of France Life Imaging network (grant ANR‐17‐ CE18‐0030, VERISMO project).References
1. Varma, G. et al. Interpretation of magnetization transfer from inhomogeneously broadened
lines (ihMT) in tissues as a dipolar order effect within motion restricted
molecules. J. Magn. Reson. 260, 67–76 (2015).
2. Prevost, V. H. et al.
Optimization of inhomogeneous magnetization transfer (ihMT) MRI contrast for
preclinical studies using dipolar relaxation time (T1D) filtering. NMR
Biomed. 30, e3706 (2017).
3. Varma, G. et al.
Three‐dimensional inhomogeneous magnetization transfer with rapid gradient‐echo
(3D ihMTRAGE) imaging. Magn. Reson. Med. (2020) doi:10.1002/mrm.28324.
4. Varma, G. et al.
In vivo measurement of a new source of contrast, the dipolar relaxation time, T
1 D , using a modified inhomogeneous magnetization
transfer (ihMT) sequence: In Vivo Measurement of T 1D Using ihMT. Magn.
Reson. Med. 78, 1362–1372 (2017).
5. Carvalho, V. N. D. et
al. MRI assessment of multiple dipolar relaxation time ( T 1 D ) components
in biological tissues interpreted with a generalized inhomogeneous
magnetization transfer (ihMT) model. J. Magn. Reson. 311, 106668 (2020).
6. Varma, G. et al.
Low duty-cycle pulsed irradiation reduces magnetization transfer and increases
the inhomogeneous magnetization transfer effect. J. Magn. Reson. 296, 60–71 (2018).