Lexiaozi Fan1, Ye Tian2, Ganesh Adluru3,4, Jason Mendes3, Li-Yueh Hsu5, Jane E. Wilcox6, Edward DiBella3,4, Daniel C. Lee6, and Daniel Kim1,7
1Department of Radiology, Northwestern University Feinberg School of Medicine, Chicago, IL, United States, 2Ming Hsieh Department of Electrical and Computer Engineering, University of Southern California, Los Angeles, CA, United States, 3Utah Center for Advanced Imaging Research (UCAIR), Department of Radiology and Imaging Sciences, University of Utah, Salt Lake City, UT, United States, 4Department of Biomedical Engineering, University of Utah, Salt Lake City, UT, United States, 5Department of Radiology and Imaging Sciences, National Institutes of Health, Bethesda, MD, United States, 6Division of Cardiology, Internal Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL, United States, 7Department of Biomedical Engineering, Northwestern University, Evanston, IL, United States
Synopsis
Keywords: Myocardium, Perfusion, Simultaneous multi-slice, myocardial blood flow
Motivation: While simultaneous multi-slice (SMS) excitation has been proposed to increase the myocardial coverage for cardiac perfusion MRI, its influence on the quantification of myocardial blood flow (MBF) has not been evaluated.
Goal(s): To determine whether SMS with multiband factor of two preserves accuracy in the quantification of MBF compared with the corresponding perfusion MRI with single-slice excitation.
Approach: We prospectively enrolled six patients and performed standard and SMS perfusion MRI back-to-back and calculated the arterial input function (AIF) and resting MBF.
Results: Both the AIF and MBF values calculated from the datasets acquired with the two perfusion sequences were comparable.
Impact: This
study demonstrates feasibility of utilizing a 2D simultaneous multi-slice (SMS)
(multiband factor = 2) perfusion sequence to increase the myocardial coverage and
quantify the myocardial blood flow to help coronary artery disease diagnosis.
Introduction
First-pass cardiac perfusion MRI is a
clinically indicated test for diagnosing coronary artery disease (CAD). In
patients with indeterminant coronary lesions, multi-vessel disease, and
microvascular disease, myocardial blood flow (MBF) quantification may increase
the diagnostic accuracy1 and also adds prognostic value2, 3. A limitation of cardiac perfusion MRI is the limited myocardial
coverage (e.g., 3 short-axis slices per heartbeat), which leaves little room to
overcome potential image artifacts such as the dark rim. One approach to
increase myocardial coverage is combining several acceleration techniques such
as simultaneous multi-slice (SMS) excitation, parallel imaging, compressed
sensing, and radial sampling, as previously described 4, 5, including two studies which evaluated MBF quantification using
SMS5, 6, with one comparing two SMS sequences (0.58±0.07 vs 0.61±0.16 ml/g/min) and
the other comparing an SMS to a 3D sequence (0.69±0.16 vs 0.69±0.15 ml/g/min). The purpose of this study was
to additionally incorporate self-calibration of arterial input function (AIF)7 and self-correction for T2* effects on AIF8 and evaluate the resulting SMS pulse sequence (multiband
factor = 2) against standard 2D radial pulse sequence in patients back to back.Methods
Human
Subjects & Pulse Sequence: We prospectively enrolled 6 subjects (58±7 years, 3 males) and
performed standard radial perfusion and SMS sequences back-to-back in this
order (~5 min gap) with administration
of 0.1 mmol/kg of gadobutrol at
3 mL/s via a power injector per
scan. MRI was performed on a 1.5T whole-body MRI scanner (MAGNETOM
Aera, Siemens Healthineers, Erlangen, Germany). Both perfusion sequences
had matching image parameters, except the SMS factor, including: FOV=384x384 mm2,
acquisition matrix=256x256, spatial resolution=1.5x1.5 mm2,
slice thickness=8 mm, TE/TR=1.5/3.03 ms, flip angle=15°, minimum TS=10 ms, B1-insensitive
hybrid pulse train as the saturation pulse9, electrocardiogram triggering every heartbeat, receiver bandwidth=750 Hz/pixel, 42
rays per frame (corresponding to an acceleration factor of 6.1), 5th
Fibonacci sequence of golden angles (=32.0397°)10, single-shot readout duration=128 ms, 100 repetitions. Each patient was instructed
to breathe normally during scanning. Depending on the heart rate, 3-4 slices for
standard and 6-8 slices for SMS were acquired per heartbeat, respectively.
Image reconstruction and quantification: The undersampled data were reconstructed
using a similar compressed sensing (CS) framework11, except for the phase demodulation and modulation in the
SMS reconstruction pipeline4 (Figure 1). We applied k-space image weighted contrast (KWIC) filters as a pre-processing
step prior to CS12 reconstruction of AIF and tissue
function (TF) images from the same raw k-space data11. Temporal total variation (TTV) was used as the sparsifying
transforms. Normalized
regularization weight for TTV was optimized for standard (0.01) and SMS (0.015)
perfusion data, respectively. Pixel-wise
resting MBF maps were quantified using the following steps: motion
correction13, signal normalization by the proton density weighted
image, signal to T1 conversion based on the Bloch equation14, T1 to gadolinium concentration ([Gd]) conversion assuming
fast water exchange15, T2* correction to the AIF8, [Gd] to MBF conversion based on a
Fermi model16. For
efficiency, we limited the resting MBF analyses to three short axis planes (base, mid,
apex) and then divided them into 16 AHA segments.
Statistical analysis: We tested for normality of the peak AIF
and mean MBF from 16 AHA segments using the Shapiro-Wilk test and compared
them between the standard and SMS groups using the
two-tailed, paired t-test (Wilcoxon signed-rank, if not normally distributed). The
Bland-Altman analysis were conducted to determine the levels of agreement in
peak AIF and mean MBF. A p < 0.05 was considered statistically significant. Results
The SMS perfusion sequence with
multiband factor of two enabled twice as many slices to be obtained compared to
the standard sequence (SMS: 6-8 slices vs standard: 3-4 slices).
Figure 2 showed the AIF
curves, resting MBF maps, and the corresponding bulls-eye plots representing
the mean MBF in 16 AHA segments of one representative patient. There was no significant difference (p=0.37)
in the peak AIF (standard: 13.72±1.19 vs SMS: 14.08±1.92 mM). While there was a
significant difference (*p=0.001) in mean MBF (standard: 0.76±0.11 vs SMS: 0.73
± 0.11 ml/g/min), the difference was only 4% of the mean (i.e., within the noise level). According
to the Bland-Altman analysis (Figure 3), mean
difference in AIF was 0.36 mM (2.61%) and in MBF was - 0.03 ml/g/min (-3.86%). Conclusion
The SMS radial sequence with multiband factor of two
is able to increase the myocardial coverage while maintaining accurate MBF quantification
compared with the standard radial perfusion sequence. A future study including a larger cohort of patients and including adenosine
is warranted to more thoroughly evaluate the accuracy of MBF quantification
derived from SMS data.Acknowledgements
This work is
supported by the National Institutes of Health (R01HL116895, 1R01HL167148‐01A1, R01HL151079,
R21EB030806A1), the Radiological Society of North America (EILTC2302), and the American
Heart Association (19IPLOI34760317, 949899, 903375). References
1. Mordini
FE, Haddad T, Hsu LY, Kellman P, Lowrey TB, Aletras AH, Bandettini WP and Arai
AE. Diagnostic accuracy of stress perfusion CMR in comparison with quantitative
coronary angiography: fully quantitative, semiquantitative, and qualitative
assessment. JACC Cardiovasc Imaging.
2014;7:14-22.
2. Brown LAE, Onciul SC, Broadbent DA,
Johnson K, Fent GJ, Foley JRJ, Garg P, Chew PG, Knott K, Dall'Armellina E,
Swoboda PP, Xue H, Greenwood JP, Moon JC, Kellman P and Plein S. Fully
automated, inline quantification of myocardial blood flow with cardiovascular
magnetic resonance: repeatability of measurements in healthy subjects. J Cardiovasc Magn Reson. 2018;20:48.
3. Knott KD, Seraphim A, Augusto JB,
Xue H, Chacko L, Aung N, Petersen SE, Cooper JA, Manisty C, Bhuva AN, Kotecha
T, Bourantas CV, Davies RH, Brown LAE, Plein S, Fontana M, Kellman P and Moon
JC. The Prognostic Significance of Quantitative Myocardial Perfusion: An
Artificial Intelligence-Based Approach Using Perfusion Mapping. Circulation. 2020;141:1282-1291.
4. Tian Y, Mendes J, Pedgaonkar A,
Ibrahim M, Jensen L, Schroeder JD, Wilson B, DiBella EVR and Adluru G.
Feasibility of multiple-view myocardial perfusion MRI using radial simultaneous
multi-slice acquisitions. PLoS One.
2019;14:e0211738.
5. Tian Y, Mendes J, Wilson B, Ross A,
Ranjan R, DiBella E and Adluru G. Whole-heart, ungated, free-breathing,
cardiac-phase-resolved myocardial perfusion MRI by using Continuous Radial
Interleaved simultaneous Multi-slice acquisitions at sPoiled steady-state
(CRIMP). Magn Reson Med.
2020;84:3071-3087.
6. Huang Q, Tian Y, Mendes J, Ranjan R,
Adluru G and DiBella E. Quantitative myocardial perfusion with a hybrid 2D
simultaneous multi-slice sequence. Magn
Reson Imaging. 2023;98:7-16.
7. Naresh NK, Haji-Valizadeh H, Aouad
PJ, Barrett MJ, Chow K, Ragin AB, Collins JD, Carr JC, Lee DC and Kim D.
Accelerated, first-pass cardiac perfusion pulse sequence with radial k-space
sampling, compressed sensing, and k-space weighted image contrast
reconstruction tailored for visual analysis and quantification of myocardial
blood flow. Magn Reson Med.
2019;81:2632-2643.
8. Fan L, Allen BD, Culver AE, Hsu LY,
Hong K, Benefield BC, Carr JC, Lee DC and Kim D. A theoretical framework for
retrospective T 2 * correction to the arterial input function in quantitative
myocardial perfusion MRI. Magn Reson Med.
2021;86:1137-1144.
9. Kim D, Oesingmann N and McGorty K.
Hybrid adiabatic-rectangular pulse train for effective saturation of
magnetization within the whole heart at 3 T. Magn Reson Med. 2009;62:1368-78.
10. Wundrak S, Paul J, Ulrici J, Hell E,
Geibel MA, Bernhardt P, Rottbauer W and Rasche V. Golden ratio sparse MRI using
tiny golden angles. Magnetic resonance in
medicine : official journal of the Society of Magnetic Resonance in Medicine /
Society of Magnetic Resonance in Medicine. 2016;75:2372-8.
11. Fan L, Hong K, Hsu LY, Carr JC, Allen
BD, Lee DC and Kim D. Optimal saturation recovery time for minimizing the
underestimation of arterial input function in quantitative cardiac perfusion
MRI. Magn Reson Med. 2022;88:832-839.
12. Lustig M, Donoho D and Pauly JM. Sparse
MRI: The application of compressed sensing for rapid MR imaging. Magn Reson Med. 2007;58:1182-95.
13. Benovoy M, Jacobs M, Cheriet F, Dahdah
N, Arai AE and Hsu LY. Robust universal nonrigid motion correction framework
for first-pass cardiac MR perfusion imaging. J Magn Reson Imaging. 2017;46:1060-1072.
14. Mendes JK, Adluru G, Likhite D, Fair
MJ, Gatehouse PD, Tian Y, Pedgaonkar A, Wilson B and DiBella EVR. Quantitative
3D myocardial perfusion with an efficient arterial input function. Magn Reson Med. 2020;83:1949-1963.
15. Donahue KM, Weisskoff RM and Burstein
D. Water diffusion and exchange as they influence contrast enhancement. J Magn Reson Imaging. 1997;7:102-10.
16. Jerosch-Herold
M, Wilke N and Stillman AE. Magnetic resonance quantification of the myocardial
perfusion reserve with a Fermi function model for constrained deconvolution. Medical physics. 1998;25:73-84.