Measurement techniques for magnetic resonance imaging of fast relaxing nuclei

In this review article, techniques for sodium (23Na) magnetic resonance imaging (MRI) are presented. These techniques can also be used to image other nuclei with short relaxation times (e.g., 39K, 35Cl, 17O). Twisted projection imaging, density-adapted 3D projection reconstruction, and 3D cones are preferred because of uniform k-space sampling and ultra-short echo times. Sampling density weighted apodization can be applied if intrinsic filtering is desired. This approach leads to an increased signal-to-noise ratio compared to postfiltered acquisition in cases of short readout durations relative to T2* relaxation time. Different MR approaches for anisotropic resolution are presented, which are important for imaging of thin structures such as myocardium, cartilage, and skin. The third part of this review article describes different methods to put more weighting either on the intracellular or the extracellular sodium signal by means of contrast agents, relaxation-weighted imaging, or multiple-quantum filtering.

[1]  R. Kim,et al.  Physiological basis for potassium (39K) magnetic resonance imaging of the heart. , 1999, Circulation research.

[2]  R. Lenkinski,et al.  Sodium MRI of a human transplanted kidney. , 2009, Academic radiology.

[3]  D. Noll,et al.  Homodyne detection in magnetic resonance imaging. , 1991, IEEE transactions on medical imaging.

[4]  K R Thulborn,et al.  Comprehensive MR imaging protocol for stroke management: tissue sodium concentration as a measure of tissue viability in nonhuman primate studies and in clinical studies. , 1999, Radiology.

[5]  Armin M Nagel,et al.  Performance of sampling density‐weighted and postfiltered density‐adapted projection reconstruction in sodium magnetic resonance imaging , 2013, Magnetic resonance in medicine.

[6]  K. Thulborn,et al.  Characterization and correction of system delays and eddy currents for MR imaging with ultrashort echo‐time and time‐varying gradients , 2009, Magnetic resonance in medicine.

[7]  V. Stein,et al.  Molecular structure and physiological function of chloride channels. , 2002, Physiological reviews.

[8]  Christian Beaulieu,et al.  Relationship between sodium intensity and perfusion deficits in acute ischemic stroke , 2011, Journal of magnetic resonance imaging : JMRI.

[9]  Paul A Bottomley,et al.  Tissue sodium concentration in myocardial infarction in humans: a quantitative 23Na MR imaging study. , 2008, Radiology.

[10]  Christian Beaulieu,et al.  Advantage of sampling density weighted apodization over postacquisition filtering apodization for sodium MRI of the human brain , 2008, Magnetic resonance in medicine.

[11]  C. Chung,et al.  Optimum detection of biexponential relaxation using multiple-quantum filtration techniques , 1990 .

[12]  F E Boada,et al.  Quantitative in vivo tissue sodium concentration maps: The effects of biexponential relaxation , 1994, Magnetic resonance in medicine.

[13]  L. Schad,et al.  Two‐dimensional radial sodium heart MRI using variable‐rate selective excitation and retrospective electrocardiogram gating with golden angle increments , 2013, Magnetic resonance in medicine.

[14]  J. Tukey,et al.  An algorithm for the machine calculation of complex Fourier series , 1965 .

[15]  L. Schad,et al.  Reduction of B(0) inhomogeneity effects in triple-quantum-filtered sodium imaging. , 2010, Journal of magnetic resonance.

[16]  J. Keltner,et al.  Three-dimensional triple-quantum-filtered imaging of 0.012 and 0.024 M sodium-23 using short repetition times. , 1994, Journal of magnetic resonance. Series B.

[17]  P. Jakob,et al.  Dynamics of 23Na during completely balanced steady-state free precession. , 2006, Journal of magnetic resonance.

[18]  J Hennig,et al.  Spiral reconstruction by regridding to a large rectilinear matrix: A practical solution for routine systems , 1999, Journal of magnetic resonance imaging : JMRI.

[19]  Ernesto Staroswiecki,et al.  In vivo sodium imaging of human patellar cartilage with a 3D cones sequence at 3 T and 7 T , 2010, Journal of magnetic resonance imaging : JMRI.

[20]  Tiejun Zhao,et al.  High‐resolution sodium imaging of human brain at 7 T , 2012, Magnetic resonance in medicine.

[21]  Michael Bock,et al.  3D radial projection technique with ultrashort echo times for sodium MRI: Clinical applications in human brain and skeletal muscle , 2007, Magnetic resonance in medicine.

[22]  Jeffrey L. Duerk,et al.  Analytical resolution and noise characteristics of linearly reconstructed magnetic resonance data with arbitraryk‐space sampling , 1995, Magnetic resonance in medicine.

[23]  Sodium imaging by gradient reversal , 1986 .

[24]  Daniel Brenner,et al.  Simultaneous single‐quantum and triple‐quantum‐filtered MRI of 23Na (SISTINA) , 2013, Magnetic resonance in medicine.

[25]  Thomas H. Mareci,et al.  Essential considerations for spectral localization using indirect gradient encoding of spatial information , 1991 .

[26]  Wolfhard Semmler,et al.  The Potential of Relaxation-Weighted Sodium Magnetic Resonance Imaging as Demonstrated on Brain Tumors , 2011, Investigative radiology.

[27]  D I Hoult,et al.  The signal-to-noise ratio of the nuclear magnetic resonance experiment. 1976. , 1976, Journal of magnetic resonance.

[28]  A. Haase,et al.  FLASH imaging: rapid NMR imaging using low flip-angle pulses. 1986. , 1986, Journal of magnetic resonance.

[29]  D G Nishimura,et al.  Twisting radial lines with application to robust magnetic resonance imaging of irregular flow , 1992, Magnetic resonance in medicine.

[30]  S K Hilal,et al.  In vivo NMR imaging of tissue sodium in the intact cat before and after acute cerebral stroke. , 1983, AJNR. American journal of neuroradiology.

[31]  R. Jennings,et al.  Electrolyte Alterations in Acute Myocardial Ischemic Injury , 1964, Circulation research.

[32]  Lau Pc,et al.  Image formation by induced local interactions. Examples employing nuclear magnetic resonance. 1973. , 1989 .

[33]  P A Bottomley,et al.  Human skeletal muscle: sodium MR imaging and quantification-potential applications in exercise and disease. , 2000, Radiology.

[34]  Yi Zhang,et al.  In vitro and in vivo studies of 17O NMR sensitivity at 9.4 and 16.4 T , 2013, Magnetic resonance in medicine.

[35]  S. Wimperis,et al.  Triple-quantum sodium imaging , 1991 .

[36]  F. Boada,et al.  Triple-quantum-filtered imaging of sodium in presence of B(0) inhomogeneities. , 2005, Journal of magnetic resonance.

[37]  N. Shah,et al.  B0 insensitive multiple-quantum resolved sodium imaging using a phase-rotation scheme. , 2013, Journal of magnetic resonance.

[38]  Michael Garwood,et al.  Fast and quiet MRI using a swept radiofrequency. , 2006, Journal of magnetic resonance.

[39]  Qing Huo Liu,et al.  Least-Square NUFFT Methods Applied to 2-D and 3-D Radially Encoded MR Image Reconstruction , 2009, IEEE Transactions on Biomedical Engineering.

[40]  Lothar R. Schad,et al.  Quantitative and qualitative (23)Na MR imaging of the human kidneys at 3 T: before and after a water load. , 2011, Radiology.

[41]  Yongxian Qian,et al.  Acquisition‐weighted stack of spirals for fast high‐resolution three‐dimensional ultra‐short echo time MR imaging , 2008, Magnetic resonance in medicine.

[42]  F. Boada,et al.  Three‐dimensional triple‐quantum–filtered 23Na imaging of in vivo human brain , 1999, Magnetic resonance in medicine.

[43]  D Hahn,et al.  Assessment of myocardial infarction in humans with (23)Na MR imaging: comparison with cine MR imaging and delayed contrast enhancement. , 2001, Radiology.

[44]  Dwight G Nishimura,et al.  Design and analysis of a practical 3D cones trajectory , 2006, Magnetic resonance in medicine.

[45]  John S. Leigh,et al.  Selective detection of intracellular sodium by coherence-transfer NMR , 1987 .

[46]  Lawrence L Wald,et al.  Sodium imaging of human brain at 7 T with 15‐channel array coil , 2012, Magnetic resonance in medicine.

[47]  Robin K. Harris,et al.  NMR Nomenclature: Nuclear Spin Properties and Conventions for Chemical Shifts—IUPAC Recommendations , 2002 .

[48]  N. Oesingmann,et al.  B0 inhomogeneity‐insensitive triple‐quantum‐filtered sodium imaging using a 12‐step phase‐cycling scheme , 2010, NMR in biomedicine.

[49]  F. Harris On the use of windows for harmonic analysis with the discrete Fourier transform , 1978, Proceedings of the IEEE.

[50]  Lothar R Schad,et al.  In vivo(39)K, (23)Na and (1)H MR imaging using a triple resonant RF coil setup. , 2009, Journal of magnetic resonance.

[51]  Wolfhard Semmler,et al.  3 Tesla Sodium Inversion Recovery Magnetic Resonance Imaging Allows for Improved Visualization of Intracellular Sodium Content Changes in Muscular Channelopathies , 2011, Investigative radiology.

[52]  N J Pelc,et al.  Reduction of motion artifacts in cine MRI using variable‐density spiral trajectories , 1997, Magnetic resonance in medicine.

[53]  K. Thulborn,et al.  Impact of gradient timing error on the tissue sodium concentration bioscale measured using flexible twisted projection imaging. , 2011, Journal of magnetic resonance.

[54]  Friedrich Wetterling,et al.  Apparent Diffusion Coefficient and Sodium Concentration Measurements in Human Prostate Tissue via Hydrogen-1 and Sodium-23 Magnetic Resonance Imaging in a Clinical Setting at 3 T , 2012, Investigative radiology.

[55]  Wolfhard Semmler,et al.  Sodium MRI using a density‐adapted 3D radial acquisition technique , 2009, Magnetic resonance in medicine.

[56]  Armin M Nagel,et al.  In vivo 39K MR imaging of human muscle and brain. , 2013, Radiology.

[57]  J Hennig,et al.  Reduced circular field‐of‐view imaging , 1998, Magnetic resonance in medicine.

[58]  Ian C. Atkinson,et al.  Feasibility of mapping the tissue mass corrected bioscale of cerebral metabolic rate of oxygen consumption using 17-oxygen and 23-sodium MR imaging in a human brain at 9.4T , 2010, NeuroImage.

[59]  J. B. Kneeland,et al.  Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI. , 2000, Osteoarthritis and cartilage.

[60]  S. Neubauer,et al.  Time course of 23Na signal intensity after myocardial infarction in humans , 2004, Magnetic resonance in medicine.

[61]  J M Pauly,et al.  Lung parenchyma: projection reconstruction MR imaging. , 1991, Radiology.

[62]  Peder E. Z. Larson,et al.  Anisotropic Field-of-Views in Radial Imaging , 2021, IEEE Transactions on Medical Imaging.

[63]  Keith R Thulborn,et al.  Feasibility of 39‐potassium MR imaging of a human brain at 9.4 Tesla , 2014, Magnetic resonance in medicine.

[64]  Konstantin V. Romanenko,et al.  (35)Cl profiling using centric scan SPRITE with variable flip angle excitation. , 2009, Journal of magnetic resonance.

[65]  Lothar R. Schad,et al.  ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times , 2004, Magnetic Resonance Materials in Physics, Biology and Medicine.

[66]  J. Pauly,et al.  Boron‐11 imaging with a three‐dimensional reconstruction method , 1992, Journal of magnetic resonance imaging : JMRI.

[67]  Raj K. Gupta,et al.  Direct observation of resolved resonances from intra- and extracellular sodium-23 ions in NMR studies of intact cells and tissues using dysprosium(III)tripolyphosphate as paramagnetic shift reagent☆ , 1982 .

[68]  J. D. O'Sullivan,et al.  A Fast Sinc Function Gridding Algorithm for Fourier Inversion in Computer Tomography , 1985, IEEE Transactions on Medical Imaging.

[69]  I. Smith,et al.  Selection of coherence transfer pathways by pulsed‐field gradients in nmr spectroscopy , 1995 .

[70]  B Stoeckel,et al.  Brain tissue sodium concentration in multiple sclerosis: a sodium imaging study at 3 tesla. , 2010, Brain : a journal of neurology.

[71]  Andrew J Wheaton,et al.  Proteoglycan loss in human knee cartilage: quantitation with sodium MR imaging--feasibility study. , 2004, Radiology.

[72]  K. Thulborn,et al.  Spectrally weighted twisted projection imaging: Reducing T2 signal attenuation effects in fast three‐dimensional sodium imaging , 1997, Magnetic resonance in medicine.

[73]  Peter Börnert,et al.  Three‐dimensional radial ultrashort echo‐time imaging with T2 adapted sampling , 2006, Magnetic resonance in medicine.

[74]  A. Macovski,et al.  Variable-rate selective excitation , 1988 .

[75]  F E Boada,et al.  Fast three dimensional sodium imaging , 1997, Magnetic resonance in medicine.

[76]  Friedrich Wetterling,et al.  Chemical shift sodium imaging in a mouse model of thromboembolic stroke at 9.4 T , 2011, Journal of magnetic resonance imaging : JMRI.

[77]  A. Sherry,et al.  In vivo Na‐23 MR imaging and spectroscopy of rat brain during TmDOTP5− infusion , 1992, Journal of magnetic resonance imaging : JMRI.

[78]  Geoffrey Bodenhausen,et al.  Multiple-quantum NMR , 1980 .

[79]  Paul A Bottomley,et al.  Tissue sodium concentration in human brain tumors as measured with 23Na MR imaging. , 2003, Radiology.

[80]  T. Chenevert,et al.  Proton and sodium MRI assessment of emerging tumor chemotherapeutic resistance , 2006, NMR in biomedicine.

[81]  Costin Tanase,et al.  Loss of cell ion homeostasis and cell viability in the brain: what sodium MRI can tell us. , 2005, Current topics in developmental biology.

[82]  H. Berendsen,et al.  THE OBSERVATION AND GENERAL INTERPRETATION OF SODIUM MAGNETIC RESONANCE IN BIOLOGICAL MATERIAL , 1973, Annals of the New York Academy of Sciences.

[83]  Oliver Bieri,et al.  23Na MR imaging at 7 T after knee matrix-associated autologous chondrocyte transplantation preliminary results. , 2010, Radiology.

[84]  A. Macovski,et al.  Selection of a convolution function for Fourier inversion using gridding [computerised tomography application]. , 1991, IEEE transactions on medical imaging.

[85]  Janusz Hankiewicz,et al.  17O magnetic resonance imaging of the human brain , 2004, Neurological research.

[86]  Aiming Lu,et al.  Quantitative sodium imaging with a flexible twisted projection pulse sequence , 2010, Magnetic resonance in medicine.

[87]  David Howe,et al.  Qualitative and Quantitative , 2014 .

[88]  J. B. Kneeland,et al.  Sodium MRI of human articular cartilage in vivo , 1998, Magnetic resonance in medicine.

[89]  Aiming Lu,et al.  Quantitative sodium MR imaging and sodium bioscales for the management of brain tumors. , 2009, Neuroimaging clinics of North America.

[90]  Dana C Peters,et al.  Centering the projection reconstruction trajectory: Reducing gradient delay errors , 2003, Magnetic resonance in medicine.

[91]  C. Slichter Principles of magnetic resonance , 1963 .

[92]  Michael Garwood,et al.  Continuous SWIFT. , 2012, Journal of magnetic resonance.

[93]  Yi Zhang,et al.  In vivo 17O NMR approaches for brain study at high field , 2005, NMR in biomedicine.

[94]  G. Shires,et al.  Thulium 1,4,7,10-tetraazacyclododecane-1,4,7,10-tetrakis(methylene phosphonate) as a 23Na shift reagent for the in vivo rat liver. , 1993, Biochemistry.

[95]  R. N Jones I – PHYSICAL CHEMISTRY DIVISION: Report of President , 1977 .

[96]  C. Beaulieu,et al.  Signal‐to‐noise optimization for sodium MRI of the human knee at 4.7 Tesla using steady state , 2011, Magnetic resonance in medicine.

[97]  A. Nuttall Some windows with very good sidelobe behavior , 1981 .

[98]  A. Borthakur,et al.  In vivo triple quantum filtered twisted projection sodium MRI of human articular cartilage. , 1999, Journal of magnetic resonance.

[99]  Walter F Block,et al.  Time‐resolved contrast‐enhanced imaging with isotropic resolution and broad coverage using an undersampled 3D projection trajectory , 2002, Magnetic resonance in medicine.

[100]  Arijitt Borthakur,et al.  23Na MRI accurately measures fixed charge density in articular cartilage , 2002, Magnetic resonance in medicine.

[101]  Alexej Jerschow,et al.  Sodium inversion recovery MRI of the knee joint in vivo at 7T. , 2010, Journal of magnetic resonance.

[102]  D. Nishimura,et al.  Fast Three Dimensional Magnetic Resonance Imaging , 1995, Magnetic resonance in medicine.

[103]  Christian Beaulieu,et al.  Sodium imaging intensity increases with time after human ischemic stroke , 2009, Annals of neurology.

[104]  P. Styles,et al.  Triple-quantum-filtration NMR imaging of 200 mM sodium at 1.9 Tesla , 1992 .

[105]  Kamil Ugurbil,et al.  Simplified Methods for Calculating Cerebral Metabolic Rate of Oxygen Based on 17O Magnetic Resonance Spectroscopic Imaging Measurement during a Short 17O2 Inhalation , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[106]  G. Bodenhausen,et al.  Multiple‐quantum NMR spectroscopy of S=3/2 spins in isotropic phase: A new probe for multiexponential relaxation , 1986 .

[107]  M. O’Donnell,et al.  NMR imaging in the presence of magnetic field inhomogeneities and gradient field nonlinearities. , 1985, Medical physics.

[108]  J. Ra,et al.  In Vivo NMR Imaging of Sodium‐23 in the Human Head , 1985, Journal of computer assisted tomography.

[109]  Lothar R Schad,et al.  In vivo chlorine‐35, sodium‐23 and proton magnetic resonance imaging of the rat brain , 2010, NMR in biomedicine.

[110]  Robert E Lenkinski,et al.  Sodium MRI of the human kidney at 3 Tesla , 2006, Magnetic resonance in medicine.

[111]  Kamil Ugurbil,et al.  Development of 17O NMR approach for fast imaging of cerebral metabolic rate of oxygen in rat brain at high field , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[112]  E. Saff,et al.  Minimal Discrete Energy on the Sphere , 1994 .

[113]  P. Lauterbur,et al.  Image Formation by Induced Local Interactions: Examples Employing Nuclear Magnetic Resonance , 1973, Nature.

[114]  J. Cuppen,et al.  Reducing MR imaging time by one-sided reconstruction , 1987 .

[115]  Denise Davis,et al.  Sodium MR imaging of acute and subacute stroke for assessment of tissue viability. , 2005, Neuroimaging clinics of North America.

[116]  Wolfhard Semmler,et al.  Three‐dimensional biexponential weighted 23Na imaging of the human brain with higher SNR and shorter acquisition time , 2013, Magnetic resonance in medicine.

[117]  R. Gropler,et al.  Cardiac 17O MRI: Toward direct quantification of myocardial oxygen consumption , 2010, Magnetic resonance in medicine.

[118]  Weili Lin,et al.  A fast, iterative, partial-fourier technique capable of local phase recovery , 1991 .

[119]  C. Clark,et al.  Sodium MR Imaging Detection of Mild Alzheimer Disease: Preliminary Study , 2009, American Journal of Neuroradiology.

[120]  F Wenz,et al.  Imaging of Tumor Viability in Lung Cancer: Initial Results Using 23Na-MRI , 2012, Fortschritte auf dem Gebiet der Röntgenstrahlen und der bildgebenden Verfahren.

[121]  Keith R Thulborn,et al.  Safety of human MRI at static fields above the FDA 8T guideline: Sodium imaging at 9.4T does not affect vital signs or cognitive ability , 2007, Journal of magnetic resonance imaging : JMRI.

[122]  H. Naritomi,et al.  In vivo measurements of intra- and extracellular Na+ and water in the brain and muscle by nuclear magnetic resonance spectroscopy with shift reagent. , 1987, Biophysical journal.

[123]  K R Thulborn,et al.  Quantitative tissue sodium concentration mapping of the growth of focal cerebral tumors with sodium magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[124]  Bertrand Audoin,et al.  Distribution of brain sodium accumulation correlates with disability in multiple sclerosis: a cross-sectional 23Na MR imaging study. , 2012, Radiology.

[125]  C. Beaulieu,et al.  Evaluation of B0-inhomogeneity correction for triple-quantum-filtered sodium MRI of the human brain at 4.7 T. , 2013, Journal of magnetic resonance.

[126]  Dwight G. Nishimura,et al.  Rapid gridding reconstruction with a minimal oversampling ratio , 2005, IEEE Transactions on Medical Imaging.

[127]  Paul S. Hubbard,et al.  Nonexponential Nuclear Magnetic Relaxation by Quadrupole Interactions , 1970 .

[128]  Peter Bachert,et al.  A measurement setup for direct 17O MRI at 7 T , 2011, Magnetic resonance in medicine.

[129]  Christian Beaulieu,et al.  In vivo sodium magnetic resonance imaging of the human brain using soft inversion recovery fluid attenuation , 2005, Magnetic resonance in medicine.

[130]  D. Fieno,et al.  Theoretical basis for sodium and potassium MRI of the human heart at 1.5 T , 1997, Magnetic resonance in medicine.

[131]  P. Winter,et al.  TmDOTP5– as a 23Na shift reagent for the subcutaneously implanted 9L gliosarcoma in rats , 2001, Magnetic resonance in medicine.

[132]  Geng Liu,et al.  Rapid computation of sodium bioscales using gpu‐accelerated image reconstruction , 2013, Int. J. Imaging Syst. Technol..

[133]  M. Weisfeldt,et al.  Rapid in vivo monitoring of chemotherapeutic response using weighted sodium magnetic resonance imaging. , 2000, Clinical cancer research : an official journal of the American Association for Cancer Research.

[134]  R. R. Ernst,et al.  Coherence transfer echoes , 1978 .

[135]  Keith R Thulborn,et al.  Vital signs and cognitive function are not affected by 23‐sodium and 17‐oxygen magnetic resonance imaging of the human brain at 9.4 T , 2010, Journal of magnetic resonance imaging : JMRI.

[136]  Jeffrey A. Fessler,et al.  Nonuniform fast Fourier transforms using min-max interpolation , 2003, IEEE Trans. Signal Process..

[137]  Simon Konstandin,et al.  Two‐dimensional radial acquisition technique with density adaption in sodium MRI , 2011, Magnetic resonance in medicine.