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Whole-heart, ungated, free-breathing myocardial perfusion MRI by using CRIMP
Ye Tian1, Jason Mendes1, Brent Wilson2, Alexander Ross2, Edward DiBella1, and Ganesh Adluru1
1Radiology, University of Utah, Salt Lake City, UT, United States, 2Cardiology, University of Utah, Salt Lake City, UT, United States

Synopsis

We propose Continuous Radial Interleaved simultaneous Multi-slice acquisitions at sPoiled steady-state (CRIMP) for whole-heart, ungated, free-breathing myocardial perfusion assessment. The simultaneous multi-slice (SMS) sequence captures multiple cardiac phases in all image slices simultaneously and keeps the inner slices at steady-state. We use a patch-based motion-compensated locally low-rank method to reconstruct the images. Quantitative perfusion analysis was also performed with an arterial input function estimated from a separate low-dose injection.

Introduction

Myocardial perfusion MRI is an important tool to detect coronary artery disease. The clinical standard sequence requires a reliable ECG-gating signal, has limited slice coverage, and different cardiac phases in different slices. To address these limitations, we propose Continuous Radial Interleaved simultaneous Multi-slice acquisitions at sPoiled steady-state (CRIMP) that combines radial trajectory, simultaneous multi-slice (SMS), interleaving slice groups, and spoiled gradient echo (SPGR) readout. The sequence runs continuously without ECG-gating, breath-holding, or magnetization preparation (such as with a saturation recovery pulse). The sequence captures multiple cardiac phases in all of the image slices and keeps the magnetization of the inner slices in steady-state in spite of motion. The current work improves upon (1) by (i) using a novel reconstruction method, (ii) studying motion effects on the SPGR signal and (iii) performing perfusion quantification. We tested the sequence on 7 patients at both stress and rest, and performed a dual-bolus (2) scan at rest for quantitative analysis.

Methods

Pulse Sequence
The sequence interleaves three or four radial SMS slice groups ($$$N_{\mathrm{SG}}$$$) as shown in Figure 1. CAIPIRINHA (3) phase modulation is applied with a multi-slice factor $$$N_{\mathrm{SMS}}=3$$$, resulting in a total of 9 or 12 image slices. We apply a golden angle sampling (4) within each slice group, and use an offset angle of $$$111.25°/N_{\mathrm{SG}}$$$ between slice groups. All studies were performed on a 3T Prisma (Siemens) scanner with parameters: TR/TE=5.9/0.8ms, FOV=260mm2, voxel size=1.8x1.8x5-8mm3 and FA=14°-15°.

Reconstruction
Image reconstruction was performed in two stages. In the first stage, we obtained preliminary images with a high temporal resolution for cardiac self-gating. We used the RING method (5) to correct for gradient delay errors. We then used a sliding-window that slides 6 rays and uses 12 rays/time frame to sort the data, achieving a temporal resolution of 32ms with a temporal footprint of 68ms. The sorted radial SMS k-space was interpolated onto a Cartesian grid by SMS-GROG (6). A temporally constrained reconstruction was used separately for each slice group (SG) by minimizing the cost function:
$$\underset{m_{\mathrm{SG}}}{\mathrm{argmin}}\left\Vert{A}m_{\mathrm{SG}}-d_{\mathrm{SG}}\right\Vert^2_2+\lambda_{t,\mathrm{SG}}\left\Vert\sqrt{(\nabla_tm_{\mathrm{SG}})^2}+\epsilon\right\Vert_1,(1)$$
where $$$A=\Phi DFS$$$ is the forward sampling matrix including sensitivity maps $$$S$$$, Fourier transform $$$F$$$, undersampling mask $$$D$$$, and phase modulation $$$\Phi$$$. $$$\lambda_{t,\mathrm{SG}}=0.04C$$$ with $$$C$$$ being the highest pixel intensity in the initial estimation $$$A^Hd_{\mathrm{SG}}$$$. The cardiac signal was automatically extracted from the preliminary images as shown in Figure 2. By using the cardiac signal, the radial k-space data was sorted to have a fixed number of cardiac phases in each cardiac cycle. Then motion-compensated patch-based total variation and locally low-rank regularizations were applied on each cardiac phase and included in the cost function in eq. (1) to finish the reconstruction, with all slices reconstructed jointly:
$$\underset{m}{\mathrm{argmin}}\left\Vert{A}m-d'\right\Vert^2_2+\lambda_t\left\Vert\sqrt{(\nabla_tm)^2}+\epsilon\right\Vert_1+\lambda_t\sum_{i=1}^{N_{\mathrm{patch}}}\left\Vert\sqrt{(\nabla_{t,\mathrm{cycle}}\mathcal{P}_i)^2+\epsilon}\right\Vert_1+\sum_{i=1}^{N_{\mathrm{patch}}}\left\Vert\mathcal{P}_i\right\Vert_*,s.t.\mathcal{P}_i=P_i(m).(2) $$
$$$\mathcal{P}_i=P_i(m)$$$ (of size $$$5\times5\times2\times{N}_{\mathrm{cycle}}$$$) represents the $$$i$$$th patch series extracted from the image $$$m$$$, and $$$\left\Vert\cdot\right\Vert_*$$$ is the nuclear norm. An ADMM algorithm (7) was used to solve the cost function in eq. (2).

Simulation of Motion Effects on the Steady-State Signal
A potential issue with the SPGR readout is that the steady-state signal is sensitive to motion (8). We performed simulations to show that motion effects in CRIMP are ignorable for inner slices. A sinusoidal motion model with different heartrates and maximum displacements were used in the simulation.

Quantification
We obtained tissue curves from the CRIMP acquired images. The AIF was estimated from a separate diluted matched volume low-dose (0.0075mmol/L, 1/10 of the normal dose) injection acquired with a saturation recovery sequence proposed previously (6,9). Both the tissue and AIF signal intensity (SI) curves were converted to gadolinium concentration using a look-up-table created from Bloch simulations. CRIMP signal intensities were corrected for B1 inhomogeneity. We then fit the gadolinium curves to a two-compartment model to obtain the myocardial blood flow (MBF) values.

Results

Simulation of Motion Effects on the Steady-State Signal
The results summarized in Figure 3 show that the inner slices are less affected by motion than the outermost slices.

CRIMP acquired images with perfusion deficits
A total of 7 patients were scanned with CRIMP at both stress and rest. Figure 4 shows a subject with infarct acquired with 12 slices ($$$N_{\mathrm{SG}}=4$$$ and $$$N_{\mathrm{SMS}}=3$$$) and slice thickness=5mm. Figure 4(a) shows self-gated systolic images at myocardial enhancement for both stress and rest. Orange arrows point to perfusion deficits seen on the stress images. Figure 4(b) shows post-T1 and late enhancement images with a closely matched slice 7 with perfusion deficits.

Quantitative MBF
Figure 5 shows the systolic MBF maps estimated from the dual-bolus rest scan. Figure 5(a) shows pixelwise MBF and Figure 5(b) shows corresponding bullseye plots with segmentation according to the AHA 17-segment model (10). The averages MBF value is 0.64±0.15.

Discussion

CRIMP sequence can provide whole-heart coverage at multiple cardiac phases for first-pass myocardial perfusion without any ECG-gating or breath-holding, which has potential clinical benefits. However, the current reconstruction time requires ~3 hours, making the sequence less practical when timing is important. Another drawback of CRIMP is that the blood pool is affected by inflow effects, requiring a separate saturation recovery sequence to obtain the AIF. Given the whole-heart coverage with multiple cardiac phases and high SNR (1), the CRIMP sequence is advantageous for qualitative myocardial perfusion assessment.

Acknowledgements

This research was supported by the National Heart Lung and Blood Institute of the National Institutes of Health under award number RO1HL138082.

References

1. Tian Y, Mendes J, Wilson B, DiBella E, Adluru G. Whole heart ungated myocardial perfusion imaging with steady-state radial SMS readout and without magnetization preparation. 2019; Montréal, QC, Canada. In Proceedings of the 27th Annual Meeting of ISMRM. p 1234.

2. Christian TF, Aletras AH, Arai AE. Estimation of absolute myocardial blood flow during first-pass MR perfusion imaging using a dual-bolus injection technique: comparison to single-bolus injection method. J Magn Reson Imaging 2008;27(6):1271-1277.

3. Yutzy SR, Seiberlich N, Duerk JL, Griswold MA. Improvements in multislice parallel imaging using radial CAIPIRINHA. Magn Reson Med 2011;65(6):1630-1637.

4. Winkelmann S, Schaeffter T, Koehler T, Eggers H, Doessel O. An optimal radial profile order based on the Golden Ratio for time-resolved MRI. IEEE Trans Med Imaging 2007;26(1):68-76.

5. Rosenzweig S, Holme HCM, Uecker M. Simple auto-calibrated gradient delay estimation from few spokes using Radial Intersections (RING). Magn Reson Med 2019;81(3):1898-1906.

6. Tian Y, Mendes J, Pedgaonkar A, Ibrahim M, Jensen L, Schroeder JD, Wilson B, DiBella EVR, Adluru G. Feasibility of multiple-view myocardial perfusion MRI using radial simultaneous multi-slice acquisitions. PLoS One 2019;14(2):e0211738.

7. Boyd S, Parikh N, Chu E, Peleato B, Eckstein J. Distributed Optimization and Statistical Learning via the Alternating Direction Method of Multipliers. Found Trends Mach Learn 2011;3(1):1-122.

8. DiBella EV, Chen L, Schabel MC, Adluru G, McGann CJ. Myocardial perfusion acquisition without magnetization preparation or gating. Magn Reson Med 2012;67(3):609-613.

9. Wang H, Adluru G, Chen L, Kholmovski EG, Bangerter NK, DiBella EV. Radial simultaneous multi-slice CAIPI for ungated myocardial perfusion. Magn Reson Imaging 2016;34(9):1329-1336.

10. Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, Pennell DJ, Rumberger JA, Ryan T, Verani MS, American Heart Association Writing Group on Myocardial S, Registration for Cardiac I. Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart. A statement for healthcare professionals from the Cardiac Imaging Committee of the Council on Clinical Cardiology of the American Heart Association. Int J Cardiovasc Imaging 2002;18(1):539-542.

Figures

Figure 1. Illustration of CRIMP with interleaving 3 SMS slice groups. Each slice group consists of 3 simultaneously excited and acquired short-axis slices, with a gap of 2-slice thicknesses. The top left image shows the slice coverage on a 4-chamber view image. The sequence continuously reads out rays by interleaving the 3 slice groups. Golden-ratio sampling is applied as illustrated in the figure. CAIPI phase modulation is applied on the 3 simultaneously acquired slices. Readout time of each ray is ~2ms providing a TR of ~6ms for each slice group.

Figure 2. Flowchart of the reconstruction process. After the pre-processing of radial SMS k-space, a temporally constrained reconstruction was performed to obtain preliminary images. An ROI in each slice that includes the blood pools were automatically detected by thresholding the standard deviation map. The pixels in the ROI were summed, and then bandpass filtered to be the cardiac signal. Then the radial k-space was sorted to have a fixed number of cardiac phases in each cardiac cycle. A patch-based reconstruction was applied to the sorted k-space to finish the reconstruction.

Figure 3. Motion simulation results. (a) shows the slice profile used in-vivo and in the simulation. (b) shows the longitudinal magnetization, Mz (T1 = 300ms) evolution with slice selective alpha pulses with or without motion. We used a sinusoidal motion with heartrate = 120/min and maximum displacement = 1 slice thickness (ST). (c) shows the read out SI curves from subfigure (b). (d) shows the signal variation (SImax - SImin)/SImean in the tail of subfigure (c) for different T1 and motion states. The results show that the inner slices are less affected by motion than the outermost slices.

Figure 4. A disease case acquired with interleaving 4 slice groups and SMS factor of 3, resulting in 12 slices. Subfigure (a) shows a peak contrast enhanced time frame for all of the slices at both stress and rest. In the stress images, perfusion deficits are seen on multiple slices and are pointed by orange arrows. Subfigure (b) shows post contrast T1 map and late enhancement images with closely matched slice 7 where perfusion deficits are seen.

Figure 5. Quantitative MBF results. Subfigure (a) shows self-gated systolic pixelwise MBF maps for 7 slices. We discarded the most apical and basal slices since they are the edge slices affected by motion. Subfigure (b) shows the bullseye plot of the MBF values. The overall averaged MBF value is 0.64±0.15.

Proc. Intl. Soc. Mag. Reson. Med. 28 (2020)
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