Synopsis
Over the last few decades, the advent of high
and ultra-high field MRI and the growing availability of novel sequence
acquisition schemes have led to substantial advances in sodium 23 (23Na)
imaging and have rekindled interest in clinical applications. Advantages and disadvantages associated with the
use of 23Na MRI will be discussed. The contribution of 23Na
MRI to a better understanding of the pathophysiology of neurological diseases
and the potential clinical impact of sodium measurements in terms of diagnosis
and prognosis will also be discussed. Finally, future directions to pursue in
this research field will be identified
Over the last few decades, the advent of high and ultra-high
field MRI and the growing availability of novel sequence acquisition schemes have
led to substantial advances in sodium 23 (23Na) imaging and have rekindled
interest in clinical applications (1).
From a biological point of view, the 23Na ion has
a critical role in several cellular functions such as mitosis, cellular
proliferation, generation and propagation of action potentials and cell volume
regulation (2). To ensure the maintenance of tissue homeostasis and the
preservation of intracellular structures and processes, 23Na
concentration is strictly controlled by the ATP-driven Na/K pump; pathological
changes that determine an expansion of the extracellular space (e.g. tissue
injury, edema or necrosis) or functional impairment of the Na/K pump are
therefore expected to result in an increased tissue 23Na
concentration (2).
From an MRI point of view, 23Na yields
the second strongest nuclear magnetic resonance (NMR) signal among all
biologically relevant NMR-active nuclei. However, the average concentration of
Na ions in brain and the sensitivity of the 23Na nucleus is much
lower than that of protons. In most biological tissues, sodium can be separated
in two compartments: extra-cellular and intra-cellular. The extracellular
sodium concentration (ESC) is ~ 140 mmol/L and the intracellular sodium
concentration (ISC) is ~ 15 mmol/L. The ability of the cell to maintain a
sodium gradient across the cell membrane, sodium ion homeostasis, can be used
as an operational definition of tissue viability. The observed average sodium
concentration is composed of the weighted average of ESC and ISC in the brain
tissue, which is around 20% and 80%, respectively (3-7).
Measurements
of total sodium concentration (TSC) obtained using 23Na MRI can be
useful in measuring tissue viability in patients with stroke (7) and cell
infiltration in patients with brain tumors (8). More recently, it has been
shown that, in patients with epilepsy, a chronic TSC elevation is associated
with the epileptogenic region even during the interictal period (9). Finally, our
and other groups have shown that 23Na MRI is feasible in patients
with multiple sclerosis (MS) and have reported the presence and clinical
relevance of TSC abnormalities in MS patients with different phenotypes (10-14).
Since TSC is an average of ESC and ISC, SQ 23Na MRI does not allow discrimination
between the two concentrations, especially the ISC which is physiologically
most relevant (15).
Advantages
and disadvantages associated with the use of 23Na MRI will be
discussed. The contribution of 23Na MRI to a better understanding of
the pathophysiology of neurological diseases and the potential clinical impact
of sodium measurements in terms of diagnosis and prognosis will also be
discussed. Finally, future directions to pursue in this research field will
be identified.
This
information will benefit a large and multidisciplinary community of
neuroscientists, clinicians, physicists and bioengineers.Acknowledgements
NIH NINDS R01NS099527
References
1.Shah NJ, Worthoff WA, Langen KJ. Imaging
of sodium in the brain: a brief review. NMR Biomed. 2016; 29:162-74
2.Thulborn KR. Quantitative sodium MR
imaging: A review of its evolving role in medicine. Neuroimage 2018; 168:250-268.
3.Hancu I, Boada FE, Shen GX. Three-dimensional
triple-quantum-filtered (23)Na imaging of in vivo human brain. Magn Reson Med 1999;42:1146-54
4.Stobbe R, Beaulieu C. In vivo sodium magnetic resonance
imaging of the human brain using soft inversion recovery fluid attenuation. Magn Reson Med 2005;54:1305-10.
5.Fleysher L, Oesingmann N, Inglese M. B(0)
inhomogeneity-insensitive triple-quantum-filtered sodium imaging using a
12-step phase-cycling scheme. NMR Biomed.
2010;23:1191-8.
6.Benkhedah N et al. 3D biexponential 23Na imaging of the human
brain with higher SNR and shorter echo time. Magn Reson Med 2013; 70:754-65.
7.Thulborn KR 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. Radiology 1999;213:156-66.
8.Ouwerkerk R et al. Tissue sodium concentration in human brain
tumors as measured with 23Na MR imaging. Radiology
2003;227:529-37.
9.Ridley B. et al. Brain sodium MRI in human epilepsy:
Disturbances of ionic homeostasis
a.
reflect the organization of pathological regions. NeuroImage
157 (2017) 173–183.
10.Inglese
M, Madelin G, Oesingmann N, et al. Brain tissue sodium concentration in
multiple sclerosis: a sodium imaging study at 3 tesla. Brain 2010;27:27.
11.Petracca
M, Vancea RO, Fleysher L, Jonkman LE, Oesingmann N, Inglese M. Brain intra- and
extracellular sodium concentration in multiple sclerosis: a 7 T MRI study. Brain 2016, 139: 795-806.
12.Zaaraoui
W, Konstandin S, Audoin B, et al. Distribution of brain sodium accumulation
correlates with disability in multiple sclerosis: a cross-sectional 23Na MR
imaging study. Radiology. 2012;264:859-67.
13.Paling
D, Solanky BS, Riemer F, et al. Sodium accumulation is associated with
disability and a progressive course in multiple sclerosis. Brain. 2013;136:2305-17.
14.Eisele
P, Konstandin S, Griebe M, et al. Heterogeneity of acute multiple sclerosis
lesions on sodium (23Na) MRI. Mult Scler 2015.
15.Fleysher
L, Oesingmann N, Brown R, Sodickson DK, Wiggins GC, Inglese M. Noninvasive
quantification of intracellular sodium in human brain using ultrahigh-field
MRI. NMR Biomed. 2013;26:9-19.