Features of sodium magnetic resonance spectroscopy and its application in neurology

Cover Page


Cite item

Full Text

Abstract

Magnetic resonance spectroscopy is an important non-invasive method that measures concentration and spatial distribution of certain biochemically significant tissue metabolites. This relatively new method has now evolved from a research tool to an independent diagnostic neuroimaging method, which provides answers to a number of important clinical and diagnostic questions at the early stages of the disease, and allows evaluation of treatment efficacy and determination of clinical outcome.

The article provides a review of data on sodium magnetic resonance spectroscopy, which is a very sensitive method for assessing cell viability and ion homeostasis. It can be used to measure early biochemical disturbances in the tissues in various degenerative diseases. We describe pathophysiology and technology underlying sodium magnetic resonance spectroscopy, as well as the most promising points of application of this method in central nervous system disorders seen by radiologists and neurologists in their clinical practice.

About the authors

Viktoriya V. Sinkova

Research Center of Neurology

Author for correspondence.
Email: kattorina@list.ru
ORCID iD: 0000-0003-2285-2725

resident, Neuroradiology department

Russian Federation, 125367 Moscow, Volokolamskoye shosse, 80

Irina A. Krotenkova

Research Center of Neurology

Email: kattorina@list.ru
ORCID iD: 0000-0001-5823-9434

Cand. Sci. (Med.), researcher, Neuroradiology department

Russian Federation, 125367 Moscow, Volokolamskoye shosse, 80

Alina A. Lyaskovik

Research Center of Neurology

Email: kattorina@list.ru
ORCID iD: 0000-0001-8062-0784

resident, Neuroradiology department

Russian Federation, 125367 Moscow, Volokolamskoye shosse, 80

Rodion N. Konovalov

Research Center of Neurology

Email: kattorina@list.ru
ORCID iD: 0000-0001-5539-245X

Cand. Sci. (Med.), senior researcher, Neuroradiology department

Russian Federation, 125367 Moscow, Volokolamskoye shosse, 80

Marina V. Krotenkova

Research Center of Neurology

Email: kattorina@list.ru
ORCID iD: 0000-0003-3820-4554

D. Sci. (Med.), Head, Neuroradiology department

Russian Federation, 125367 Moscow, Volokolamskoye shosse, 80

References

  1. Khomenko I.G., Bogdan A.A., Kataeva G.V., Chernysheva E.M. Multivoxel magnetic resonance spectroscopy in the examination of patients with cognitive disorders. Vestnik SPbGU. Fizika i khimiya.2016;3(1):82–89.(In Russ.)
  2. Berendsen H.J., Edzes H.T. The observation and general interpretation of sodium magnetic resonance in biological material. Ann NY Acad Sci. 2017;204:459–485. doi: 10.1111/j.1749-6632.1973.tb30799.x. PMDI: 4513164.
  3. Magnuson J.A., Magnuson N.S. NMR studies of sodium and potassium in various biological tissues. Ann NY Acad Sci. 1973;204:297–309. doi: 10.1111/j.1749-6632.1973.tb30786.x. PMID: 4513156.
  4. Feinberg D.A., Crooks L.A., Kaufman L. et al. Magnetic-resonance imaging performance — a comparison of sodium and hydrogen. Radiology. 2009;156(1):133–138. doi: 10.1148/radiology.156.1.4001399. PMID: 4001399.
  5. Maudsley A.A., Hilal S.K. Biological aspects of Na-23 imaging. Br Med Bull. 1984;40(2):165–166. doi: 10.1093/oxfordjournals.bmb.a071964. PMID: 6744003.
  6. Hilal S.K., Maudsley A.A., Ra J.B. et al. In vivo NMR imaging of sodium-23 in the human head. J Comput Assist Tomogr. 1985;9(1):1–7. doi: 10.1097/00004728-198501000-00001. PMID: 3968256.
  7. Grodd W., Klose U. Sodium-MR-imaging of the brain — initial clinical-results. Neuroradiology. 2008;30(5):399–407. doi: 10.1007/BF00404105. PMID: 2850509.
  8. Boada F.E., Gillen J.S., Shen G.X. et al. Fast three dimensional sodium imaging. Magn Reson Med. 2017;37(5):706–715. doi: 10.1002/mrm.1910370512. PMID: 9126944.
  9. Jerschow A. From nuclear structure to the quadrupolar NMR interaction and high-resolution spectroscopy. Prog NMR Spectrosc. 2005;46:63–78. doi: 10.1016/j.pnmrs.2004.12.001.
  10. Jaccard G., Wimperis S., Bodenhausen G. Multiple quantum NMR-spectroscopy of S=3/2 spins in isotropic phase: a new probe for multiexponential relaxation. J Chem Phys. 2007; 5:6282–6293. doi: 10.1002/9780470034590.emrstm0336.
  11. Madelin G., Kline R., Walvick R., Regatte R.R. A method for estimating intracellular sodium concentration and extracellular volume fraction in brain in vivo using sodium magnetic resonance imaging. Sci Rep. 2010;4:4763. doi: 10.1038/srep04763. PMID: 24755879.
  12. Veen J.W., Gelderen P., Creyghton J.H., Bovée W.M. Diffusion in red blood cell suspensions: separation of the intracellular and extracellular NMR sodium signal. Magn Reson Med. 2010 Apr; 29(4):571–574. PMID: 8464377.
  13. Lundberg P., Kuchel P.W. Diffusion of solutes in agarose and alginate gels: 1H and 23Na PFGSE and 23Na TQF NMR studies. Magn Reson Med. 1997;37(1):44–52. PMID: 8978631.
  14. 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(5):1305–1310. doi: 10.1002/mrm.20696. PMID: 16217782.
  15. Madelin G., Babb J., Xia D. et al. Articular cartilage: evaluation with fluid-suppressed 7.0-T sodium MR imaging in subjects with and subjects without osteoarthritis. Radiology. 2013;268(2):481–491. doi: 10.1148/radiol.13121511. PMID: 23468572.
  16. Chang G., Madelin G., Sherman O.H. et al. Improved assessment of cartilage repair tissue using fluid-suppressed 23Na inversion recovery MRI at 7 Tesla: preliminary results. Eur Radiol. 2019;22(6):1341–1349. doi: 10.1007/s00330-012-2383-8. PMID: 22350437.
  17. Madelin G., Babb J.S., Xia D. et al. Reproducibility and repeatability of quantitative sodium magnetic resonance imaging in vivo in articular cartilage at 3 T and 7 T. Magn Reson Med. 2011;68(3):841–849. doi: 10.1002/mrm.23307. PMID: 22180051.
  18. Rooney W.D., Springer C.S. A comprehensive approach to the analysis and interpretation of the resonances of spins 3/2 from living systems. NMR Biomed. 2019; 4(5):209–226. doi: 10.1002/nbm.1940040502. PMID: 1751345.
  19. Allis J.L., Seymour A.M.L., Radda G.K. Absolute quantification of intracellular Na+ using triple-quantum-filtered sodium-23 NMR. Magn Reson. 1991;93:71–76. doi: 10.1002/mrm.23147.
  20. Madelin G., Lee J.S., Regatte R.R., Jerschow A. Sodium MRI: methods and applications. Prog Nucl Magn Reson Spectrosc. 2014;79:14–47. doi: 10.1016/j.pnmrs.2014.02.001. PMID: 24815363.
  21. Fleysher L., Oesingmann N., Brown R. et al. Noninvasive quantification of intracellular sodium in human brain using ultrahigh-field MRI. NMR Biomed. 2019;26(1):9–19. doi: 10.1002/nbm.2813. PMID: 22714793.
  22. Petracca M., Fleysher L., Oesingmann N., Inglese M. Sodium MRI of multiple sclerosis. NMR Biomed. 2016;29(2):153–161. doi: 10.1002/nbm.3289. PMID: 25851455.
  23. Biller A., Pflugmann I., Badde S. et al. Sodium MRI in multiple sclerosis is compatible with intracellular sodium accumulation and inflammation-induced hyper-cellularity of acute brain lesions. Sci Rep. 2016;6:31269. doi: 10.1038/srep31269. PMID: 27507776.
  24. Inglese M., Madelin G., Oesingmann N. et al. Brain tissue sodium concentration in multiple sclerosis: a sodium imaging study at 3 tesla. Brain. 2010;133(Pt 3):847–857. doi: 10.1093/brain/awp334. PMID: 20110245.
  25. Huhn K., Engelhorn T., Linker R.A., Nagel A.M. Potential of sodium MRI as a biomarker for neurodegeneration and neuroinflammation in multiple sclerosis. 2019;10:84. doi: 10.3389/fneur.2019.00084. PMID: 30804885.
  26. Kleinewietfeld M., Manzel A., Titze J. et al. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature. 2013;496(7446):518–22. doi: 10.1038/nature11868. PMID: 23467095.
  27. Farez M.F. Salt intake in multiple sclerosis: friend or foe? J Neurol Neurosurg Psychiatry. 2016;87(12):1276. doi: 10.1136/jnnp-2016-313768. PMID: 27352796.
  28. Fitzgerald K.C., Munger K.L., Hartung H.P. et al. Sodium intake and multiple sclerosis activity and progression in BENEFIT. Ann Neurol. 2017;82(10:20–29. doi: 10.1002/ana.24965. PMID: 28556498.
  29. Nourbakhsh B., Graves J., Casper T.C. et al. Dietary salt intake and time to relapse in paediatric multiple sclerosis. J Neurol Neurosurg Psychiatry. 2016;87(12):1350–1353. doi: 10.1136/jnnp-2016-313410. PMID: 27343226.
  30. Krotenkova M.V. Diagnosis of acute stroke: algorithms for neuroimaging studies: Thesis D. Sci. (Med.). Мoscow, 2011. 122 p. (In Russ.)
  31. Wetterling F., Gallagher L., Mullin J. et al. Sodium-23 magnetic resonance imaging has potential for improving penumbra detection but not for estimating stroke onset time. J Cereb Blood Flow Metab. 2015;35(1):103–110. doi: 10.1038/jcbfm.2014.174. PMID: 25335803.
  32. Nunes Neto L.P., Madelin G., Sood T.P. et al. Quantitative sodium imaging and gliomas: a feasibility study. Neuroradiology. 2018;60(8):795–802. doi: 10.1007/s00234-018-2041-1. PMID: 29862413.
  33. Thulborn K.R., Lu A., Atkinson I.C. et al. Quantitative sodium MR imaging and sodium bioscales for the management of brain tumors. Neuroimaging Clin N Am. 2009;19(4):615–624. doi: 10.1016/j.nic.2009.09.001. PMID: 19959008.
  34. Mellon E.A., Pilkinton D.T., Clark C.M. et al. Sodium MR imaging detection of mild Alzheimer disease: preliminary study. Am J Neuroradiol. 2009;30(5):978–984. doi: 10.3174/ajnr.A1495. PMID: 19213826.
  35. Konstandin S., Nagel A.M. Measurement techniques for magnetic resonance imaging of fast relaxing nuclei. MAGMA. 2014;27(1):5–19. doi: 10.1007/s10334-013-0394-3. PMID: 23881004.
  36. Atkinson I.C., Renteria L., Burd H. et al. Safety of human MRI at static fields above the FDA 8 T guideline: sodium imaging at 9.4 T does not affect vital signs or cognitive ability. J Magn Reson Imaging. 2017;26(5):1222–1227. doi: 10.1002/jmri.21150. PMID: 17969172.
  37. Rauschenberg J., Nagel A.M., Ladd S.C. et al. Multicenter study of subjective acceptance during magnetic resonance imaging at 7 and 9.4 T. Invest Radiol. 2014;49(5):249–59. doi: 10.1097/RLI.0000000000000035. PMID: 24637589.
  38. Kearney H., Miller D.H., Ciccarelli O. Spinal cord MRI in multiple sclerosis–diagnostic, prognostic and clinical value. Nat Rev Neurol. 2015;11(6):327–338. doi: 10.1038/nrneurol.2015.80. PMID: 26009002.
  39. Kopp C., Linz P., Dahlmann A. et al. 23Na magnetic resonance imaging-determined tissue sodium in healthy subjects and hypertensive patients. Hypertension. 2020;61:635–640. doi: 10.1161/HYPERTENSIONAHA.111.00566. PMID: 23339169.
  40. Titze J. Sodium balance is not just a renal affair. Curr Opin Nephrol Hypertens. 2014;23:101–105. doi: 10.1097/01.mnh.0000441151.55320.c3. PMID: 24401786.
  41. Wang P., Deger M.S., Kang H. et al. Sex differences in sodium deposition in human muscle and skin. Magn Reson Imaging. 2017;36:93–7. doi: 10.1016/j.mri.2016.10.023. PMID: 27989912.
  42. Kaunzner U.W., Gauthier S.A. MRI in the assessment and monitoring of multiple sclerosis: an update on best practice. Ther Adv Neurol Disord. 2017;10(6):247–261. doi: 10.1177/1756285617708911. PMID: 28607577.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2021 Sinkova V.V., Krotenkova I.A., Lyaskovik A.A., Konovalov R.N., Krotenkova M.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77-83204 от 12.05.2022.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies