Jabrane Karkouri1, Stanislav Frištyk2, Lucian AB Purvis3, Christopher T. Rodgers*1, and Ladislav Valkovic*3
1Wolfson Brain Imaging Center, University of Cambridge, Cambridge, United Kingdom, 2Department of Electromagnetic and Biomedical Engineering, University of Žilina, Zilina, Slovakia, 3Oxford Centre for Clinical Magnetic Resonance Research, University of Oxford, Oxford, United Kingdom
Synopsis
Phosphorus
magnetic resonance spectroscopy (31P-MRS) delivers unique information to aid
our understanding of cardiac metabolism. To quantify “absolute”
concentrations of phosphorus metabolites (i.e. in recognised units such as mmol
/ kg wet weight), sensitivity calibration and transmit field correction are
required. Ultrahigh field (>7 T) magnets and the use of multichannel RF
coils make this even more challenging. In this study, we investigate the
feasibility of absolute concentration of phosphorus metabolites in the human
heart at 7T, compare our findings to literature values and evaluate reproducibility
with different coils and different MR systems.
Introduction
Changes in cardiac energy metabolism are related to all
major cardiovascular disorders as well as systemic disease[1], such as obesity[2] and type-II diabetes[3]. Phosphorus
magnetic resonance spectroscopy (31P-MRS) affords unique insight into
cardiac energetics but has a low intrinsic signal-to-noise ratio (SNR) in
humans. This can be increased at 7T, enabling a better investigation of cardiac
metabolism[5]. 31P-MRS cardiac energetic
assessments are often reported in terms of the PCr/ATP concentration ratio[4]
on the assumption that ATP concentration varies little in vivo.
However, PCr/ATP is insensitive to simultaneous changes in
the concentrations of both metabolites which does occur in heart failure and other diseases. In this
study, we have investigated the feasibility to quantify absolute concentrations
of human cardiac 31P metabolites at 7T. To demonstrate the
versatility of the approach, two different MR systems and three RF coil designs
were tested. Methods
Two different 7T MR systems (Magnetom and Terra, both
Siemens Healthineers, Erlangen, Germany) equipped with two different RF coils
were used for data acquisition to demonstrate the flexibility of this absolute
quantification approach. The Magnetom MR scanner was combined with a 16-channel-receive array coil with local rectangular transmit surface coil (Rapid Biomedical,
Rimpar, Germany) (Figure 1) and the Terra MR scanner was equipped with a prototype
surface body dipole+loop array (Tesla Dynamic Coils, Zaltbommel, The
Netherlands). The surface body coil dipole array is composed of 4 Anterior and
4 posterior Tx/Rx 1H/31P dipoles and 16 31P-Rx
loops. For data acquisition, two of the dipoles A3 and A4 were used for
transmission(Figure 2).
The absolute quantification method in Purvis et
al.[6] for liver metabolites at 7T was adjusted for the heart. This required
RF field simulations for B1 distribution in several voxel models and
determination of target conductivity to be matched by the reference phantom (Figure
1). Based on the simulations, two phantoms containing 30mM K2HPO4
(jerry cans of dimensions 165x700x310 mm3 in Cambridge and 280×280×450 mm3 in Oxford) were prepared and
used for the field mapping experiments.
Field maps were acquired as a set of 31P images using a 3D-GRE sequence
over a 32×16×8 matrix and a 500×250×15 mm3 field of view.
Minimal TE (6.9ms) and a TR of 100ms were used for each image with an
increasing transmit voltage of the excitation sinc pulse in steps of 50VRMS
from 0-450VRMS.
3D-weighted-CSI cardiac data has been acquired on the heart
with TR 1s, matrix size 8x16x8, FOV 220 mm, vector size 1024 points, spectral
bandwidth 6 kHz and both 16-channel array body coil (Rapid Biomedical) and
dipole+loop array body coil (from Tesla DC). Acquisition time was 6min30s
with the 16-channel array body coil (4 averages) and 11min48s for the Tesla
DC coil (7 averages).
Data
processing:
The field
maps were generated by fitting the signal intensities acquired at different
voltages and maps of B1+ were converted in Hz/volt by multiplication of the number of degrees FA/Hz
calculated for the sinc pulse used in the GRE acquisition.
Before analysis, the single‐channel spectra were combined using WSVD[8]. Each
spectrum was analyzed using the OXSA toolbox[7]. Fitting was done using the AMARES
implemented in OXSA.
For the final absolute quantification of cardiac
metabolites, a calibration factor was calculated by scaling the mode of the
corrected amplitudes from the reference phantom scan to match the true
concentration (30mM). This calibration factor was applied to the in vivo
data.Results and Discussion
Figure 1, simulated conductivity over 3 different
voxel models are shown. The simulated conductivities of reference phantoms that
would yield the minimal RMSE vs the voxel modes were 0.52S/m for 7T, with the
error at 7T rising dramatically with minimal changes in conductivity. Purvis et
al. in their liver study found the ideal conductivities to be lower, 0.38S/m
for 7T, which reflects the lower conductivity of the liver tissue (0.5S/m) to
the cardiac muscle (0.73S/m) and the difference in the organ position and
surrounding anatomy.
Figure 3 shows B1 field map of the 16-channel array coil and
Tesla DC dipole array coil, both for transmission and sensitivity.
Figure 4 shows a fit result for a voxel in the myocardium
with AMARES and an ATP absolute concentration map obtained with the Tesla DC
dipole body array coil for the Terra MR system.
Figure 5 shows the same results but obtained in Oxford with
the Rapid Biomedical 16-channel array coil.
An ATP concentration of 4.80 ± 1.06 mmol/kg wet weight was obtained
in the heart using data acquired on either MR system. This is in good agreement
with literature[9] and demonstrates good versatility of the proposed approach
since two different systems were used. More direct comparison using the same
volunteers will be performed once all 8 dipoles can be used for transmit
simultaneously.Conclusion
After adjusting the reference phantom conductivity based on
EM simulations, we have demonstrated feasibility of the method originally
proposed for absolute quantification of liver metabolites at 7T by Purvis et al. to provide concentration of
cardiac energy metabolites, such as ATP. The demonstrated potential of method
to be independent on the MR system of RF coil used could make it very
attractive for widespread use, moving 7T cardiac 31P-MRS from
evaluating PCr/ATP towards absolute concentrations.Acknowledgements
Jabrane Karkouri is funded by the
European Union’s Horizon 2020 research and innovation programme under
grant agreement No 801075.
Christopher T. Rodgers and Ladislav Valkovic are funded by a Sir Henry Dale Fellowship from
the Wellcome Trust and the Royal Society [098436/Z/12/B].
This study was funded by the NIHR Cambridge
Biomedical Research Centre and MRC Clinical Research Infrastructure Award for
7T.
Support of the Slovak Grant
Agencies VEGA [2/0003/20] and
APVV [19–0032] is also gratefully acknowledged.
Stanislav Frištyk
would like to acknowledge the support of the NSP of Slovakia.
References
[1] Hudsmith, Lucy E., and Stefan
Neubauer. "Magnetic resonance spectroscopy in myocardial
disease." JACC: Cardiovascular Imaging 2.1 (2009): 87-96.
[2] Rayner, Jennifer J., et al. "Myocardial
energetics in obesity: enhanced ATP delivery through creatine kinase with
blunted stress response." Circulation 141.14 (2020):
1152-1163.
[3] Levelt, Eylem, et al.
"Ectopic and visceral fat deposition in lean and obese patients with type
2 diabetes." Journal of the American College of Cardiology 68.1
(2016): 53-63.
[4] Bottomley, Paul A., et al. "Metabolic
rates of ATP transfer through creatine kinase (CK Flux) predict clinical heart
failure events and death." Science translational medicine 5.215
(2013): 215re3-215re3.
[5] Rodgers, Christopher T., et al. "Human cardiac 31P
magnetic resonance spectroscopy at 7 Tesla." Magnetic resonance in
medicine 72.2 (2014): 304-315.
[6] Purvis LAB, Valkovič L, Robson
MD, Rodgers CT. Feasibility of absolute quantification for 31 P
MRS at 7 T. Magn Reson Med. 2019;82(1):49-61. doi:10.1002/mrm.27729
[7] Purvis LAB, Clarke WT, Biasiolli
L, Valkovic L, Robson MD, Rodgers CT. OXSA: an
open‐source magnetic resonance spectroscopy analysis toolbox in MATLAB. PLoS ONE. 2017;12:e0185356.
[8] Rodgers,
Christopher T., and Matthew D. Robson. "Receive array magnetic resonance spectroscopy:
whitened singular value decomposition (WSVD) gives optimal Bayesian
solution." Magnetic Resonance in Medicine: An Official Journal of
the International Society for Magnetic Resonance in Medicine 63.4
(2010): 881-891.
[9] Kemp,
Graham J., Martin Meyerspeer, and Ewald Moser. "Absolute quantification of
phosphorus metabolite concentrations in human muscle in vivo by 31P MRS: a
quantitative review." NMR in Biomedicine: An International Journal
Devoted to the Development and Application of Magnetic Resonance in Vivo 20.6
(2007): 555-565.