Kirsten Koolstra1, Andrew Webb1, and Peter Börnert1,2
1Leiden University Medical Center, Leiden, Netherlands, 2Philips Research Hamburg, Hamburg, Germany
Synopsis
Fast relaxation
time quantification is important in dynamic muscle studies and can
be achieved using Magnetic Resonance Fingerprinting (MRF). The T2
values in muscle measured with MRF are consistently higher than those
measured with the conventionally used multi-echo turbo-spin-echo (MSE) method,
while T1 values are closer to reference measurements. We hypothesize that this increase can in part be attributed to an increased
sensitivity of MRF to flow compared to MSE. In this work we
test the sensitivity of MRF to flow in muscle by saturating a slab at different distances above the imaging slice for variable suppression
of inflowing spins.
Introduction
Fast relaxation
time quantification is important in dynamic muscle studies1.
Recently it was shown that Magnetic Resonance Fingerprinting2 (MRF) can
provide T1, T2, M0 and FF (fat fraction) maps
simultaneously in approximately 15 seconds per slice3, supporting
time-resolved exercise studies4. The water T2 values in
muscle measured with MRF, however, were consistently higher (~31% difference) than
those measured with the conventionally used multi-echo turbo-spin-echo (MSE)
method5 (Figure 1a), even when high time-bandwidth RF pulses are
used in MRF. MRF T1 values in muscle were much closer to those
obtained with the reference inversion recovery (IR) method (~7% difference). Other
studies have also found a mismatch between MRF and standard techniques6,7,
but the source of these discrepancies is not yet understood. One clear
difference between MRF and MSE is the much larger number of excitation pulses used
for MRF compared to MSE. During such a long excitation/sampling period new spins
that flow into the imaging slice will contribute to the final MRF signal. Therefore,
our hypothesis is that the increased MRF water T2 in muscle can in
part be attributed to an increased sensitivity to flow-related processes
compared to MSE. In this work we perform initial in-vivo experiments to test
the sensitivity of MRF to in-flow in muscle. We do this by applying a spatial
saturation pulse at different distances above the imaging slice for variable
suppression of inflowing spins. We investigate the difference in estimated T1/T2
values with respect to those obtained with a saturation pulse below the imaging
slice, to eliminate magnetization transfer (MT) effects.Methods
Experiments were
performed with informed consent obtained, using an Ingenia 3T MR system
(Philips Healthcare) equipped with a quadrature transmit 16-channel receive
knee coil. For one volunteer the sensitivity to flow was analyzed at rest by adding
a spatial saturation pulse to each of the individual MRF pulses, suppressing a
60 mm thick region (saturation slab) above or below the imaging slice at five
different distances (5,10,15,20,50 mm). The scan was repeated with a zero degree RF saturation
tip angle for reference. The setup is schematically shown in Figure
1b-c. In another volunteer the MRF T1/T2 values were
compared with the conventional MSE/IR method.
MRF definition: A pattern of 1000 flip angles8, was used
preceded by an inversion pulse. The TEs alternated between 3.45 ms and 2.30 ms,
with constant flip angle for alternating TEs to enable chemical shift encoding3.
The TR/RF-phase was fixed to 20 ms/0°.
Data acquisition: MRF data were acquired using a spoiled SSFP sequence
with a spiral sampling scheme and the following scan parameters: FOV 230x230 mm2,
resolution 1.31x1.31x10 mm3, 8 ms spiral read-out, undersampling
factor 20, scan time 20s. MSE data were acquired using a CPMG readout with
17 echoes: TR/TE/ΔTE 3000/8/8 ms, and analyzed using a tri-exponential fit9.
IR data were acquired with spectral pre-saturation fat suppression and TR/TSE
factor = 5s/16.
Dictionary and Matching: The dictionary was calculated
using the extended phase graph formalism10. 123,645 signal evolutions were
simulated with T1/T2/B1+ factors ranging from 20-2000ms/10-500ms/0.5-1.2, respectively. Before calculating
T1, T2 and M0 maps in the matching process,
the fat signal was removed from the water signal following the procedure
described in ref. 3.Results
Figure 2 shows the T1 maps for the
saturation slab below or above the imaging slice at different distances. The
values in the T1 map increase when the saturation pulse is switched
off (0⁰ RF saturation angle) due to MT effects. As the saturation slab is moved
closer to the imaging slice, the T1 values decrease further, both
due to increased MT and suppressed flow effects. Assuming a symmetric MT spectrum,
the difference T1 maps (suppression below-suppression above slice),
show larger differences when the saturated slab is closer to the imaging slice.
Figure 3 shows similar results for the T2 maps. Figure 4 summarizes
the difference T1 and T2 values averaged over an ROI (Figure 4a) in
the soleus muscle, also showing larger differences and standard
deviations for smaller distances of the saturation slab to the imaging slice:
up to ~75/9 ms for mean T1/T2, respectively. Discussion
The comparison
between saturating a region below and above the imaging slice during the MRF
scan allows us to eliminate symmetric MT effects and other confounding
symmetric effects that might be present in this set up. The remaining
difference in T1 and T2 indicates that there is a
measurable effect of flow of spins into the imaging slice. This difference is
associated with an increase in both the estimated T1 and T2
values in the analyzed ROI in the soleus muscle. The numbers confirm that percentually muscle T2 (~28%) is much
more affected by flow than muscle T1 (~8%). Future work should examine any non-symmetric
effects as confounding factors.Conclusion
We have shown a strong indication for a non-negligible effect of flow-related
processes on the matched parameter maps in muscle MRF. Such flow effects can
lead to a small increase in the estimated water T1, but a much
larger increase in estimated water T2 in muscle, and can therefore be
an explanation for the overestimation of T2 values measured with MRF
compared to those measured with MSE.Acknowledgements
This project was funded by the European Research Council Advanced Grant
670629 NOMA MRI.References
1. Varghese, J et al. Rapid assessment of quantitative T1,
T2 and T2* in lower extremity muscles in response to
maximal treadmill exercise. NMR in Biomedicine. 2015;28(8):998–1008.
2. Ma, D et al. Magnetic Resonance Fingerprinting.
Nature. 2013;495(7440):187–192.
3. Koolstra, K et al. Water-Fat Separation in Spiral
Magnetic Resonance Fingerprinting using Conjugate Phase Reconstruction. 27th
ISMRM in Paris. 2018; 0681.
4. Marty, B et al.
Physiological and Pathological Skeletal Muscle T1 changes quantified using a
fast inversion-recovery radial NMR imaging sequence. Scientific reports. 2019;9(1):6852.
5. Forbes, S et al. Magnetic Resonance Imaging and
Spectroscopy Assessment of Lower Extremity Skeletal Muscles in Boys with
Duchenne Muscular Dystrophy: A Multicenter Cross Sectional Study. PLOS ONE.
2014;9(9):1–8.
6. Marty, B et al. MR fingerprinting for water T1 and fat
fraction quantification in fat infiltrated skeletal muscles. Magnetic Resonance
in Medicine. 2019; 10.1002/mrm.27960.
7. Ma, D et al. Slice Profile and B1 Corrections in 2D
Magnetic Resonance Fingerprinting (MRF). Magnetic Resonance in Medicine. 2017;78(5):1781–1789.
8. Sommer, K et al. Towards predicting the encoding
capability of MR fingerprinting sequences. Magnetic Resonance Imaging. 2017;
41:7–14.
9. Azzabou, N et al. Validation of a Generic Approach to
Muscle Water T2 Determination at 3T in Fat-Infiltrated Skeletal Muscle. Journal
of Magnetic Resonance Imaging. 2015;41:645–653.
10. Scheffler, K. A pictorial Description of Steady-States
in Rapid Magnetic Resonance Imaging. Concepts in Magnetic Resonance.
1999;11(5):291–304.