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Three-dimensional whole-brain simultaneous quantitative mapping of T1, T2, T2*, and susceptibility with MR Multitasking
Tianle Cao1,2, Sen Ma1, Nan Wang1, Sara Gharabaghi3, Yibin Xie1, Zhaoyang Fan1,4,5, Elliot Hogg6, E. Mark Haacke 3,7,8, Michele Tagliati6, Anthony G. Christodoulou1,2, and Debiao Li1,2
1Biomedical Imaging Research Institute, Cedars Sinai Medical Center, Los Angeles, CA, United States, 2Department of Bioengineering, University of California, Los Angeles, Los Angeles, CA, United States, 3Magnetic Resonance Innovations, Inc., Bingham Farms, MI, United States, 4Department of Radiation Oncology, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States, 5Department of Radiology, University of Southern California, Los Angeles, CA, United States, 6Department of Neurology, Cedars Sinai Medical Center, Los Angeles, CA, United States, 7Department of Radiology, Wayne State University School of Medicine, Detroit, MI, United States, 8The MRI Institute for Biomedical Research, Bingham Farms, MI, United States

Synopsis

A new approach for simultaneous quantitative mapping of T1, T2, T2*, and susceptibility was developed. This technique employs hybrid T2 preparation/inversion pulse modules followed by fully flow-compensated multi-echo FLASH readouts. Our method reconstructs images with different T2 preparation times, echo times, and inversion times in the MR Multitasking framework and use them for parameter quantification. Results of both visual comparison and statistical analysis showed that our proposed method agreed well with reference methods while being more time efficient.

Introduction

MR imaging offers various image contrasts primarily weighted by proton density (PD), longitudinal relaxation time (T1) or transverse relaxation times (T2, T2*). Quantification of these parameters can reveal important information about tissue composition. For example, T1 is correlated with myelin concentration1 and axon diameter2. T1 and T2 values have been used for lesion identification in multiple sclerosis patients3. Both susceptibility and R2* are related to iron deposition in the human brain4 as a result of aging5 and neurodegenerative diseases6-8. Recently multiparametric mapping has been shown to offer better diagnostic performance9,10. However, conventional ways for multi-parametric quantification require separate scans, which are time-consuming and may suffer from inter-scan misregistration. In this work, we developed a new approach to efficient and simultaneous quantitative mapping of T1, T2, T2* and susceptibility based on MR Multitasking framework.

Methods

Sequence diagram
The sequence diagram is shown in Fig. 1a. Hybrid T2 preparation/inversion pulse modules preparation times were followed by multi-echo FLASH readouts. The readout modules acquired k-space lines at different combinations of T2 preparation time ($$$\tau=0,30,55,80ms$$$), inversion time ($$$t_{TI}=0-2880ms$$$), and echo time ($$$t_{TE}=5,10,16ms$$$). Two interleaved subsets of data were acquired for the multitasking framework: imaging data and navigator data, as shown in Fig 1c. To reduce flow-induced phase error, full flow compensation along all directions and for all echoes were implemented based on previous literature11, as shown in Fig. 1b.
Imaging model
The underlying image series can be written as a 6-dimensional low rank tensor $$$x\left(\boldsymbol{r}, \tau, t_{T I}, t_{T E}\right)$$$ with three spatial dimensions indexed by $$$\boldsymbol{r}=[x, y, z]$$$, and 3 temporal dimensions $$$\tau$$$, $$$t_{TI}$$$, and $$$t_{TE}$$$. The image can be reconstructed using a low rank tensor model12 :
$$\mathrm{x}_{(1)}=\mathrm{U}_{\mathrm{r}} \Phi$$
Where subscript (1) denotes mode-1 unfolding of the tensor, $$$U_r$$$ are spatial coefficients and $$$\Phi=\mathrm{G}_{(1)} \otimes U_{\tau} \otimes U_{T I} \otimes U_{T E}$$$ is a temporal factor consisting of a core tensor $$$G_{(1)}$$$ and corresponding basis. The temporal factor $$$\Phi$$$ can be determined from Bloch-constrained low-rank tensor completion of navigator data12, after which we recover $$$U_r$$$ by solving the following optimization problem:
$$\widehat{\mathbf{U}}_{r}=\arg \min _{\mathbf{U}_{\mathbf{r}}}\left\|\mathbf{d}_{\mathrm{img}}-\Omega(\mathbf{E} \mathbf{U} \Phi)\right\|_{2}^{2}+\lambda R\left(\mathbf{U}_{\mathbf{r}}\right)$$
where $$$d_{img}$$$ are the imaging data, $$$\Omega$$$ is an undersampling operator, $$$E$$$ combines multi-channel encoding, and $$$R\left(\mathbf{U}_{\mathbf{r}}\right)$$$ is a total variation regularizer.
Parameter quantification
The voxel-wise relaxation parameters are quantified using the following signal model:
$$S=M_{z 0} \frac{1-e^{-T_{\mathrm{R}} / T_{1}}}{1-e^{-T_{\mathrm{R}} / T_{1}} \cos \alpha}\left[1+\left(B e^{-\tau / T_{2}}-1\right)\left(e^{-T_{\mathrm{R}} / T_{1}} \cos \alpha\right)^{n}\right] e^{-t_{T E} / T_{2}^{*}} e^{j \Delta B_{0} t_{T E}} \sin \alpha$$
where $$$M_{z 0}$$$ absorbs the equilibrium magnetization, $$$B$$$ represents effective inversion efficiency, $$$\Delta B_{0}$$$ describes the static field inhomogenity, $$$T_R$$$ is the FLASH readout repetition time and $$$n$$$ represents readout index. QSM (quantitative susceptibility mapping) was computed using brain-extracted multi-echo images from the last FLASH readout module by removing background field13 and solving dipole inversion problem14.
MR experiments
Ten healthy volunteers and one Parkinson disease (PD) patient were scanned on a 3T scanner (Biograph mMR, Siemens). The data was acquired with FOV$$$=276 \times 207 \times 144 \mathrm{~mm}^{3}$$$ and voxel size$$$=1.4 \times 0.7 \times 2.0 \mathrm{~mm}^{3}$$$. The scan time was 9.13 min for 72 slices. Reference maps were collected for comparison: T1 maps (from IR-TSE, 24 slices), T2 maps (from ME-SE, 40 slices), and T2*/QSM maps (from ME-GRE, 72 slices), which took ~20 min.
Image analysis
Multitasking maps were compared qualitatively and quantitatively against the reference maps. Mean T1/T2/T2* values were calculated from cortical gray matter (GM) and white matter (WM) regions and mean susceptibility values were calculated from subcortical regions including substantia nigra (SN), red nucleus (RN), and globus pallidus (GP). Bland-Altman analysis and intra-class correlation coefficient (ICC) were used for assessment. Using all parameters, different contrast-weighted images were synthesized, including T1, double inversion recovery (DIR), T2, FLAIR, T2*, and minimum intensity projections (mIPs) of SWI/true SWI (tSWI). The Multitasking R2* and QSM maps of the PD patient were compared with an age and gender-matched healthy volunteer.

Results

Of all three slices in Fig. 2, Multitasking maps showed similar tissue contrast and features to reference maps. Bland - Altman plots in Fig. 3 showed small biases between Multitasking and reference measurements for T1 (+6%, p<0.001), T2 (-4%, p=0.002), and T2* (-5%, p=0.008) with no bias for QSM measurements. Nevertheless, parameter values from Multitasking are in agreement with literature15-21 and ICCs are above 0.75, indicating excellent consistency between Multitasking and reference methods22. Contrast-weighted images synthesized from Multitasking parametric maps are shown in Fig. 4. They show high quality and good contrast. Higher paramagnetic susceptibility and R2* were found in SN and pallidum regions of the patient, as shown in Fig. 5.

Discussion and Conclusion

In this work, we developed an efficient simultaneous T1, T2, T2*, and susceptibility mapping technique based on the MR Multitasking framework. The proposed method yielded consistent results with the references based on qualitative and statistical analysis and demonstrated its clinical feasibility. The proposed method was less time-consuming than the conventional techniques and wouldn’t suffer from inter-scan misregistration. Similar to previous Multitasking work25, the approach here can still compensate or remove motion throughout the scan, thus allowing more robust clinical applications. Scan time may be further reduced with Deep Learning and more clinical validations would be performed.

Acknowledgements

This work was supported by the National Institutes of Health (Grant/Award No. 1R01EB028146).

References

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Figures

Figure 1. a) Sequence diagram. Hybrid IR/T2IR preparations were followed by multi-echo FLASH readouts. The navigator data was acquired every 4 readouts.

b) Illustration of the readout module. After each 𝛼 pulse, a total of 3 echoes, each of them fully flow compensated along all directions, were collected in a monopolar way. In the phase/partition encoding direction, bipolar gradient pairs are added for later echoes.

c) Simplified illustration of k-space sampling pattern. Cartesian acquisition with random Gaussian distribution was used along $$$k_y$$$ and $$$k_z$$$ directions.


Figure 2. Representative T1/T2/T2*/QSM mapping at 3 slice locations using MR Multitasking and the corresponding reference protocols on a healthy volunteer.

Figure 3. Bland - Altman plots and ICC of a) T1/T2/T2* and b) QSM measurements (N=10).

Figure 4. Results from a 23-year-old female volunteer including qualitative images and quantitative data. The first row shows quantitative maps and the second and third rows show the synthesized weighted images. SWI and tSWI were minimum intensity projection (mIP) results with an effective slab thickness of 16 mm. χ1=0, χ2=450ppb was adopted for tSWI23.

R2* and QSM of a 62-year-old healthy volunteer (male) and 61-year-old PD patient (male). Here R2* (1/T2*) map was displayed instead of T2* to highlight the difference. Higher iron deposit could be inferred from brighter substantia nigra and pallidum region (red arrow) of the PD patient (R2*SN=55.9s-1, R2*GP=41.0s-1, χSN=198ppb, χGP=127ppb) compared with healthy control (R2*SN=32.6s-1, R2*GP=33.0s-1, χSN=153ppb, χGP=81ppb).

Proc. Intl. Soc. Mag. Reson. Med. 29 (2021)
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