Fast High-Resolution Metabolite Mapping in the rat Brain Using 1H-FID-MRSI at 14.1 T
Jazyk angličtina Země Velká Británie, Anglie Médium print
Typ dokumentu časopisecké články
Grantová podpora
201218
Swiss National Science Foundation - Switzerland
207935
Swiss National Science Foundation - Switzerland
CIBM Center for Biomedical Imaging
PubMed
39711201
DOI
10.1002/nbm.5304
Knihovny.cz E-zdroje
- Klíčová slova
- 1H‐FID‐MRSI, brain metabolites, magnetic resonance spectroscopic imaging, metabolite mapping, rat brain, ultra‐high field,
- MeSH
- krysa rodu Rattus MeSH
- magnetická rezonanční tomografie metody MeSH
- metabolom MeSH
- mozek * metabolismus diagnostické zobrazování MeSH
- poměr signál - šum MeSH
- potkani Sprague-Dawley MeSH
- potkani Wistar MeSH
- protonová magnetická rezonanční spektroskopie metody MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Magnetic resonance spectroscopic imaging (MRSI) enables the simultaneous noninvasive acquisition of MR spectra from multiple spatial locations inside the brain. Although 1H-MRSI is increasingly used in the human brain, it is not yet widely applied in the preclinical setting, mostly because of difficulties specifically related to very small nominal voxel size in the rat brain and low concentration of brain metabolites, resulting in low signal-to-noise ratio (SNR). In this context, we implemented a free induction decay 1H-MRSI sequence (1H-FID-MRSI) in the rat brain at 14.1 T. We combined the advantages of 1H-FID-MRSI with the ultra-high magnetic field to achieve higher SNR, coverage, and spatial resolution in the rat brain and developed a custom dedicated processing pipeline with a graphical user interface for Bruker 1H-FID-MRSI: MRS4Brain toolbox. LCModel fit, using the simulated metabolite basis set and in vivo measured MM, provided reliable fits for the data at acquisition delays of 1.30 ms. The resulting Cramér-Rao lower bounds were sufficiently low (< 30%) for eight metabolites of interest (total creatine, N-acetylaspartate, N-acetylaspartate + N-acetylaspartylglutamate, total choline, glutamine, glutamate, myo-inositol, and taurine), leading to highly reproducible metabolic maps. Similar spectral quality and metabolic maps were obtained with one and two averages, with slightly better contrast and brain coverage due to increased SNR in the latter case. Furthermore, the obtained metabolic maps were accurate enough to confirm the previously known brain regional distribution of some metabolites. The acquisitions proved high reproducibility over time. We demonstrated that the increased SNR and spectral resolution at 14.1 T can be translated into high spatial resolution in 1H-FID-MRSI of the rat brain in 13 min using the sequence and processing pipeline described herein. High-resolution 1H-FID-MRSI at 14.1 T provided robust, reproducible, and high-quality metabolic mapping of brain metabolites with minimal technical limitations.
Advanced Clinical Imaging Technology Siemens Healthineers International AG Lausanne Switzerland
Animal Imaging and Technology École Polytechnique fédérale de Lausanne Lausanne Switzerland
CIBM Center for Biomedical Imaging Lausanne Switzerland
Institute of Scientific Instruments of the CAS Brno Czech Republic
Zobrazit více v PubMed
W. Bogner, R. Otazo, and A. Henning, “Accelerated MR Spectroscopic Imaging—A Review of Current and Emerging Techniques,” NMR in Biomedicine 34, no. 5 (2021): e4314, https://doi.org/10.1002/nbm.4314.
R. A. de Graaf, In Vivo NMR Spectroscopy: Principles and Techniques, 2nd ed. (Chichester, UK: John Wiley & Sons Ltd, 2007), https://doi.org/10.1002/9780470512968.
A. A. Maudsley, O. C. Andronesi, P. B. Barker, et al., “Advanced Magnetic Resonance Spectroscopic Neuroimaging: Experts' Consensus Recommendations,” NMR in Biomedicine 34, no. 5 (2021): e4309, https://doi.org/10.1002/nbm.4309.
F. Lam, Y. Li, B. Clifford, and Z. P. Liang, “Macromolecule Mapping of the Brain Using Ultrashort‐TE Acquisition and Reference‐Based Metabolite Removal,” Magnetic Resonance in Medicine 79, no. 5 (2018): 2460–2469, https://doi.org/10.1002/mrm.26896.
W. Bogner, S. Gruber, S. Trattnig, and M. Chmelik, “High‐Resolution Mapping of Human Brain Metabolites by Free Induction Decay 1H MRSI at 7 T,” NMR in Biomedicine 25, no. 6 (2012): 873–882, https://doi.org/10.1002/nbm.1805.
A. Henning, A. Fuchs, J. B. Murdoch, and P. Boesiger, “Slice‐Selective FID Acquisition, Localized by Outer Volume Suppression (FIDLOVS) for 1H‐MRSI of the Human Brain at 7 T With Minimal Signal Loss,” NMR in Biomedicine 22, no. 7 (2009): 683–696, https://doi.org/10.1002/nbm.1366.
S. Nassirpour, P. Chang, and A. Henning, “High and Ultra‐High Resolution Metabolite Mapping of the Human Brain Using 1H FID MRSI at 9.4T,” NeuroImage 168 (2018): 211–221, https://doi.org/10.1016/j.neuroimage.2016.12.065.
B. Lanz, A. Abaei, O. Braissant, et al., “Magnetic Resonance Spectroscopy in the Rodent Brain: Experts' Consensus Recommendations,” NMR in Biomedicine 34, no. 5 (2021): e4325, https://doi.org/10.1002/nbm.4325.
G. Öz, I. Tkáč, and K. Uǧurbil, “Animal Models and High Field Imaging and Spectroscopy,” Dialogues in Clinical Neuroscience 15, no. 3 (2013): 263–278.
V. Mlynárik, I. Kohler, G. Gambarota, A. Vaslin, P. G. H. Clarke, and R. Gruetter, “Quantitative Proton Spectroscopic Imaging of the Neurochemical Profile in Rat Brain With Microliter Resolution at Ultra‐Short Echo Times,” Magnetic Resonance in Medicine 59, no. 1 (2008): 52–58, https://doi.org/10.1002/mrm.21447.
T. Delgado‐Goñi, S. Ortega‐Martorell, M. Ciezka, et al., “MRSI‐Based Molecular Imaging of Therapy Response to Temozolomide in Preclinical Glioblastoma Using Source Analysis,” NMR in Biomedicine 29, no. 6 (2016): 732–743, https://doi.org/10.1002/nbm.3521.
C. Cudalbu, “In Vivo Studies of Brain Metabolism in Animal Models of Hepatic Encephalopathy Using 1H Magnetic Resonance Spectroscopy,” Metabolic Brain Disease 28, no. 2 (2013): 167–174, https://doi.org/10.1007/s11011‐012‐9368‐9.
A. A. Althobity, N. Khan, C. J. Sandrock, et al., “Multiparametric Magnetic Resonance Imaging for Detection of Pathological Changes in the Central Nervous System of a Mouse Model of Multiple Sclerosis In Vivo,” NMR in Biomedicine 36, no. 10 (2023): e4964, https://doi.org/10.1002/nbm.4964.
J. Orije, F. Kara, C. Guglielmetti, et al., “Longitudinal Monitoring of Metabolic Alterations in Cuprizone Mouse Model of Multiple Sclerosis Using 1H‐Magnetic Resonance Spectroscopy,” NeuroImage 114 (2015): 128–135, https://doi.org/10.1016/j.neuroimage.2015.04.012.
L. H. Nilsen, T. M. Melø, O. Sæther, M. P. Witter, and U. Sonnewald, “Altered Neurochemical Profile in the McGill‐R‐Thy1‐APP Rat Model of Alzheimer's Disease: A Longitudinal In Vivo 1H MRS Study,” Journal of Neurochemistry 123, no. 4 (2012): 532–541, https://doi.org/10.1111/jnc.12003.
G. Hangel, B. Strasser, M. Považan, et al., “Ultra‐High Resolution Brain Metabolite Mapping at 7 T by Short‐TR Hadamard‐Encoded FID‐MRSI,” NeuroImage 168 (2016): 210, https://doi.org/10.1016/j.neuroimage.2016.10.043.
C. Geppert, W. Dreher, and D. Leibfritz, “PRESS‐Based Proton Single‐Voxel Spectroscopy and Spectroscopic Imaging With Very Short Echo Times Using Asymmetric RF Pulses,” Magnetic Resonance Materials in Physics, Biology and Medicine 16, no. 3 (2003): 144–148, https://doi.org/10.1007/s10334‐003‐0016‐6.
G. J. Topping, C. Hundshammer, L. Nagel, et al., “Acquisition Strategies for Spatially Resolved Magnetic Resonance Detection of Hyperpolarized Nuclei,” Magnetic Resonance Materials in Physics, Biology and Medicine 33, no. 2 (2020): 221–256, https://doi.org/10.1007/s10334‐019‐00807‐6.
I. Tkáč, Z. Starčuk, I. Y. Choi, and R. Gruetter, “In Vivo 1H NMR Spectroscopy of Rat Brain at 1 ms Echo Time,” Magnetic Resonance in Medicine 41, no. 4 (1999): 649–656, https://doi.org/10.1002/(SICI)1522‐2594(199904)41:4<649::AID‐MRM2>3.0.CO;2‐G.
C. Cudalbu, V. Mlynárik, L. Xin, and R. Gruetter, “Comparison of T1 Relaxation Times of the Neurochemical Profile in Rat Brain at 9.4 Tesla and 14.1 Tesla,” Magnetic Resonance in Medicine 62, no. 4 (2009): 862–867, https://doi.org/10.1002/mrm.22022.
A. Klauser, S. Courvoisier, J. Kasten, et al., “Fast High‐Resolution Brain Metabolite Mapping on a Clinical 3T MRI by Accelerated 1H‐FID‐MRSI and Low‐Rank Constrained Reconstruction,” Magnetic Resonance in Medicine 81, no. 5 (2019): 2841–2857, https://doi.org/10.1002/mrm.27623.
H. Barkhuijsen, R. de Beer, and D. van Ormondt, “Improved Algorithm for Noniterative Time‐Domain Model Fitting to Exponentially Damped Magnetic Resonance Signals,” Journal of Magnetic Resonance 73, no. 3 (1969): 553–557, https://doi.org/10.1016/0022‐2364(87)90023‐0.
J. Mosso, D. Simicic, K. Şimşek, R. Kreis, C. Cudalbu, and I. O. Jelescu, “MP‐PCA Denoising for Diffusion MRS Data: Promises and Pitfalls,” NeuroImage 263 (2022): 119634, https://doi.org/10.1016/j.neuroimage.2022.119634.
G. Öz, J. R. Alger, P. B. Barker, et al., “Clinical Proton MR Spectroscopy in Central Nervous System Disorders,” Radiology 270 (2014): 658–679, https://doi.org/10.1148/radiol.13130531.
M. Wilson, O. Andronesi, P. B. Barker, et al., “Methodological Consensus on Clinical Proton MRS of the Brain: Review and Recommendations,” Magnetic Resonance in Medicine 82 (2019): 527–550, https://doi.org/10.1002/mrm.27742.
D. A. Barrière, R. Magalhães, A. Novais, et al., “The SIGMA rat Brain Templates and Atlases for Multimodal MRI Data Analysis and Visualization,” Nature Communications 10, no. 1 (2019): 5699, https://doi.org/10.1038/s41467‐019‐13575‐7.
Z. Starčuk and J. Starčuková, “Quantum‐Mechanical Simulations for In Vivo MR Spectroscopy: Principles and Possibilities Demonstrated With the Program NMRScopeB,” Analytical Biochemistry 529 (2017): 79–97, https://doi.org/10.1016/j.ab.2016.10.007.
V. M. A. Govindaraju and K. Young, “Proton NMR Chemical Shifts and Coupling Constants for Brain Metabolites,” NMR in Biomedicine 13 (2000): 129–153, https://doi.org/10.1002/1099‐1492(200005)13:33.3.CO;2‐M.
V. Govind, K. Young, and A. A. Maudsley, “Corrigendum to Proton NMR Chemical Shifts and Coupling Constants for Brain Metabolites. [NMR Biomed. 13, (2000), 129‐153],” NMR in Biomedicine 28, no. 7 (2015): 923–924, https://doi.org/10.1002/nbm.3336.
D. Simicic, V. Rackayova, L. Xin, et al., “In Vivo Macromolecule Signals in Rat Brain 1H‐MR Spectra at 9.4T: Parametrization, Spline Baseline Estimation, and T2 Relaxation Times,” Magnetic Resonance in Medicine 86 (2021): 2384–2401, https://doi.org/10.1002/mrm.28910.
I. Tkáč, R. Rao, M. K. Georgieff, and R. Gruetter, “Developmental and Regional Changes in the Neurochemical Profile of the Rat Brain Determined by In Vivo 1H NMR Spectroscopy,” Magnetic Resonance in Medicine 50, no. 1 (2003): 24–32, https://doi.org/10.1002/mrm.10497.
S. W. Provencher, “Estimation of Metabolite Concentrations From Localized In Vivo Proton NMR Spectra,” Magnetic Resonance in Medicine 30, no. 6 (1993): 672–679, https://doi.org/10.1002/mrm.1910300604.
H. P. Hetherington, N. I. Avdievich, A. M. Kuznetsov, and J. W. Pan, “RF Shimming for Spectroscopic Localization in the Human Brain at 7 T,” Magnetic Resonance in Medicine 63, no. 1 (2010): 9–19, https://doi.org/10.1002/mrm.22182.
P. Balchandani and D. Spielman, “Fat Suppression for 1H MRSI at 7T Using Spectrally‐Selective Adiabatic Inversion Recovery,” Magnetic Resonance in Medicine 59, no. 5 (2008): 980–988, https://doi.org/10.1002/mrm.21537.
V. O. Boer, J. C. W. Siero, H. Hoogduin, J. S. van Gorp, P. R. Luijten, and D. W. J. Klomp, “High‐Field MRS of the Human Brain at Short TE and TR,” NMR in Biomedicine 24, no. 9 (2011): 1081–1088, https://doi.org/10.1002/nbm.1660.
I. Tkáč, D. Deelchand, W. Dreher, et al., “Water and Lipid Suppression Techniques for Advanced 1H MRS and MRSI of the Human Brain: Experts' Consensus Recommendations,” NMR in Biomedicine 34, no. 5 (2021): e4459, https://doi.org/10.1002/nbm.4459.
R. Kreis, V. Boer, I. Y. Choi, et al., “Terminology and Concepts for the Characterization of In Vivo MR Spectroscopy Methods and MR Spectra: Background and Experts' Consensus Recommendations,” NMR in Biomedicine 34, no. 5 (2021): e4347, https://doi.org/10.1002/nbm.4347.
M. F. Alf, H. Lei, C. Berthet, L. Hirt, R. Gruetter, and V. Mlynarik, “High‐Resolution Spatial Mapping of Changes in the Neurochemical Profile After Focal Ischemia in Mice,” NMR in Biomedicine 25, no. 2 (2012): 247–254, https://doi.org/10.1002/nbm.1740.
L. Hingerl, W. Bogner, P. Moser, et al., “Density‐Weighted Concentric Circle Trajectories for High Resolution Brain Magnetic Resonance Spectroscopic Imaging at 7T,” Magnetic Resonance in Medicine 79, no. 6 (2018): 2874–2885, https://doi.org/10.1002/mrm.26987.
L. Hingerl, B. Strasser, P. Moser, et al., “Clinical High‐Resolution 3D‐MR Spectroscopic Imaging of the Human Brain at 7 T,” Investigative Radiology 55, no. 4 (2020): 239–248, https://doi.org/10.1097/RLI.0000000000000626.