Li Huang1, Radhouene Neji1,2, Muhammad Sohaib Nazir1, John Whitaker1, Filippo Bosio1, Amedeo Chiribiri1, Reza Razavi1, and Sébastien Roujol1
1School of Biomedical Engineering and Imaging Sciences, Faculty of Life Sciences and Medicine, King's College London, London, United Kingdom, 2MR Research Collaborations, Siemens Healthcare Limited, Frimley, United Kingdom
Synopsis
Abnormal native myocardial T1 times are
associated with a variety of cardiomyopathies, and are widely measured by inversion-recovery-based
myocardial T1 mapping techniques such as modified Look-Locker inversion
recovery (MOLLI). These sequences are limited in patients with severe
breathholding difficulties for relatively long duration of breathholds. In this
work, we sought to develop and characterize shortened schemes using less amount
of T1-weighted images to reduce their sensitivity to imperfect breathholds.
Introduction
Abnormal native myocardial T1 times are associated with several
cardiomyopathies1. Inversion-recovery-based myocardial T1 mapping
techniques, such as modified Look-Locker inversion recovery (MOLLI)2,3,
are widely used because of their high precision, reproducibility and map
quality2-7. These techniques use ECG-triggered acquisition of 7-13
images with different T1 weightings of the same slice succeeding inversion
preparation to generate one T1 map in a single breathhold of 9-17 heartbeats2-7.
However, they may be limited in patients with severe breathholding
difficulties. In this work, shortened inversion-recovery-based myocardial T1
mapping schemes were developed and characterized.Methods
(1) Shortened schemes: In the
proposed shortened schemes, 2-5 T1-weighted images were acquired after only one
inversion pulse. For T1 fitting, a novel one-parameter (OP) fitting model as
well as a standard three-parameter (TP) fitting model2 with
Look-Locker and inversion factor corrections2,8 were used,
respectively. These schemes were thus defined as OPn (n=2-5) and TPn (n=3-5)
where n represents the image amount. They were compared to a conventional
5-(3)-3 MOLLI scheme, which is denoted as TP8.
(2) OP reconstruction: Dictionary
matching was performed using the OP fitting model created for a 100-2200ms T1
range and defined as S(TI)=1-(1+δ)e-TI/T1 with δ being the inversion
factor8 of the applied inversion pulse (non-selective hyperbolic-tangent) and TI the inversion time between the inversion preparation and image acquisition. Assuming
typical B0/B1 inhomogeneities of ±150Hz/80-100% and myocardial
T1/T2=400-1600/45ms, Bloch simulations of the inversion slice profiles were performed to determine δ=0.96. Signal polarity restoration9 and
magnitude scaling to each dictionary entry were performed for dictionary
matching.
(3) Computational validation: Accuracy
and precision of all schemes were evaluated using Bloch simulations with added
noise. Inversion and excitation slice profiles were calculated using the same
B0/B1 inhomogeneities and myocardial T1/T2 as mentioned above, and then used in
these Bloch simulations.
(4)
Experimental validation: Imaging in a 9-vial phantom10 (5 repetitive
scans) and 16 healthy volunteers (2 repetitive scans) were performed on a 1.5T
scanner (MAGNETOM Aera, Siemens Healthcare, Erlangen, Germany) using a conventional
5-(3)-3 MOLLI acquisition scheme with 2D bSSFP readout: TR/TE/α 2.70ms/1.12ms/35°,
FOV 360×306mm2, 1.4×2.1mm2 pixel, 3 slices with thickness
8mm, GRAPPA factor 2, partial Fourier factor 7/8, bandwidth 1085Hz/px, first
inversion time 100ms. Slices were in the short-axis orientation in the healthy
volunteer study. T1 times/spatial variability/repeatability of all schemes were
measured in each vial (phantom) and each myocardial segment11
(healthy volunteers). Kruskal-Wallis and ANOVA as well as Wilcoxon rank sum
tests and Student’s t-tests with Bonferroni correction were used to compare
schemes in phantom and in healthy volunteers, respectively. Additionally, OP2
and MOLLI were compared using subjective assessment of native T1 map quality and
Pearson correlation analysis. 5-point-scale qualitative scoring (1-non-diagnostic/5-excellent)
was undergone by consensus of 2 experienced cardiac MRI readers with respect to
image artifacts, myocardium/blood pool border delineation and myocardium
homogeneity12.
Results
Both simulation and phantom studies showed limited penalty of accuracy,
precision and spatial invariability of all shortened schemes compared to MOLLI,
as shown in Fig. 1 and Fig. 2 (although statistically insignificant
with p>0.71), respectively. Repeatability remained similar for all schemes in
phantom (p=0.75). Fig. 3 shows
representative example native T1 maps using all schemes. In the healthy
volunteer study (Fig. 4), all schemes led to similar native T1 times and repeatability for
myocardium (977-997ms, p=0.21 and 14-18ms, p=0.87) and blood (1583-1623ms,
p=0.79 and 7-15ms, p=0.41), while all shortened schemes yielded limited
increase of spatial variability for myocardium (56-59ms vs. 48ms, p<0.01)
and blood (60-105ms vs. 49ms, p<0.01) compared to MOLLI. OP2 and MOLLI yielded
high linear correlation between native myocardial T1 times (Pearson correlation
coefficient=0.95) and similar scores of subjective T1 map quality (4.8±0.2 vs.
4.8±0.2, p=1.00).Discussion
All proposed shortened schemes combined with the OP fitting model
resulted in similar native T1 range, limited reduction of precision and spatial
invariability, similar repeatability and similar map quality. Two-heartbeat
myocardial T1 mapping has been proposed, but was based on saturation recovery
and considerably increased spatial variability for native myocardial T1 mapping
by a factor of 2.5 when compared to MOLLI13. The mild increase by a
factor of 1.2 in spatial variability of all proposed shortened schemes compared
to MOLLI for native myocardial T1 mapping was in the same magnitude as yielded
by ShMOLLI7 (note TP5 can be seen as an approximation of ShMOLLI for
native myocardial T1 mapping).Conclusion
Compared to MOLLI, the proposed two-heartbeat OP2 scheme yields highly
linearly correlated native T1 times, similar repeatability, similar map quality
and mild loss in spatial invariability for native myocardial T1 mapping at
1.5T. This approach may be a valuable alternative for myocardial T1 mapping in
patients with limited breathholding abilities.Acknowledgements
This work was supported by the Health Innovation Challenge Fund (grant
number HICF-R10-698), a parallel funding partnership between the Department of
Health and the Wellcome Trust, the Wellcome Engineering and Physical Sciences
Research Council (EPSRC) Centre for Medical Engineering at King's College
London (WT 203148/Z/16/Z) and the EPSRC grant (EP/R010935/1). This
research was also supported by the National Institute for Health Research
(NIHR) Biomedical Research Centre based at Guy's and St Thomas' National Health
Service (NHS) Foundation Trust in partnership with King's College London, and
by the NIHR Healthcare Technology Co-operative for Cardiovascular Disease at
Guy’s and St Thomas' NHS Foundation Trust. The views expressed are those of
the authors and not necessarily those of the NHS, the NIHR or the Department of
Health.References
-
Moon
JC, Messroghli DR, Kellman P, Piechnik SK, Robson MD, Ugander M, Gatehouse PD,
Arai AE, Friedrich MG, Neubauer S, Schulz-Menger J, Schelbert EB. Myocardial T1
mapping and extracellular volume quantification: a Society for Cardiovascular
Magnetic Resonance (SCMR) and CMR Working Group of the European Society of
Cardiology consensus statement. J Cardiovasc Magn Reson. 2013;15(1):92.
- Messroghli DR, Radjenovic A, Kozerke S,
Higgins DM, Sivananthan MU, Ridgway JP. Modified Look-Locker inversion recovery
(MOLLI) for high-resolution T1 mapping of the heart. Magn Reson Med. 2004;52(1):141-146.
- Messroghli
DR, Niendorf T, Schulz-Menger J, Dietz R, Friedrich MG. T1 mapping in patients with acute
myocardial infarction. J Cardiovasc Magn Reson. 2003;5(2):353-359.
- Roujol S, Weingärtner S, Foppa M, Chow
K, Kawaji K, Ngo LH, Kellman P, Manning WJ, Thompson RB, Nezafat R. Accuracy,
precision, and reproducibility of four T1 mapping sequences: a head-to-head
comparison of MOLLI, ShMOLLI, SASHA, and SAPPHIRE. Radiology.
2014;272(3):683-689.
- Kellman P, Hansen MS. T1-mapping in the
heart: accuracy and precision. J Cardiovasc Magn Reson. 2014;16(1):2.
- Weingärtner
S, Meßner NM, Budjan J, Loßnitzer D, Mattler U, Papavassiliu T, Zöllner FG,
Schad LR. Myocardial T
1-mapping at 3T using saturation-recovery: reference values, precision and
comparison with MOLLI. J Cardiovasc Magn Reson. 2017;18(1):84.
- Piechnik SK, Ferreira VM, Dall'Armellina
E, Cochlin LE, Greiser A, Neubauer S, Robson MD. Shortened Modified Look-Locker
Inversion recovery (ShMOLLI) for clinical myocardial T1-mapping at 1.5 and 3 T
within a 9 heartbeat breathhold. J Cardiovasc Magn Reson. 2010;12(1):69.
- Kellman P,
Herzka DA, Hansen MS. Adiabatic
inversion pulses for myocardial T1 mapping. Magn Reson Med.
2014;71(4):1428-1434.
- Xue H, Greiser A, Zuehlsdorff S, Jolly
MP, Guehring J, Arai AE, Kellman P. Phase-sensitive inversion recovery for
myocardial T1 mapping with motion correction and parametric fitting. Magn Reson
Med. 2013;69(5):1408-1420.
- Captur G, Gatehouse P, Keenan KE,
Heslinga FG, Bruehl R, Prothmann M, Graves MJ, Eames RJ, Torlasco C, Benedetti
G, Donovan J, Ittermann B, Boubertakh R, Bathgate A, Royet C, Pang W, Nezafat
R, Salerno M, Kellman P, Moon JC. A medical device-grade T1 and ECV
phantom for global T1 mapping quality assurance-the T1 mapping and ECV
standardization in cardiovascular magnetic resonance (T1MES) program. J
Cardiovasc Magn Reson. 2016;18:58.
- Cerqueira MD, Weissman NJ, Dilsizian V,
Jacobs AK, Kaul S, Laskey WK, Pennell DJ, Rumberger JA, Ryan T, Verani MS. 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.
Circulation. 2002;105(4):539-542.
- Kellman P, Wilson JR, Xue H, Ugander M,
Arai AE. Extracellular volume fraction mapping in the myocardium, part 1:
evaluation of an automated method. J Cardiovasc Magn Reson. 2012;14:63.
- Fitts M, Breton E, Kholmovski EG,
Dosdall DJ, Vijayakumar S, Hong KP, Ranjan R, Marrouche NF, Axel L, Kim D.
Arrhythmia insensitive rapid cardiac T1 mapping pulse sequence. Magn Reson Med.
2013;70(5):1274-1282.