Noninvasive quantification of intracellular sodium in human brain using ultrahigh-field MRI

NMR in Biomedicine

Volumn 26, Issue 1, 2013, Pages 9-19

  Fleysher, Lazar ^a,b   Oesingmann, Niels ^c   Brown, Ryan ^b   Sodickson, Daniel K ^b   Wiggins, Graham C ^b   Inglese, Matilde ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

Brain; Intracellular; MR imaging; Multiple quantum filtering; Sodium; Ultrahigh magnetic field

Indexed keywords

EXTRACELLULAR; HEALTHY HUMANS; HUMAN BRAIN; IN-VIVO; IN-VIVO MEASUREMENT; INTRACELLULAR; MOLAR FRACTIONS; MR IMAGING; QUANTITATIVE ASSESSMENTS; QUANTITATIVE MEASUREMENT; TISSUE SODIUM CONCENTRATION; TISSUE VIABILITY; ULTRA-HIGH; ULTRA-HIGH MAGNETIC FIELDS;

BRAIN; ENZYME ACTIVITY; MAGNETIC RESONANCE IMAGING; OXYGEN VACANCIES; TISSUE;

SODIUM;

SODIUM;

ADULT; AGED; ARTICLE; BRAIN; BRAIN MAPPING; CELL FRACTIONATION; CELL VOLUME; CONTROLLED STUDY; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; IN VIVO STUDY; INTRACELLULAR MEMBRANE; INTRACELLULAR SODIUM CONCENTRATION; INTRACELLULAR SODIUM MOLAR FRACTION; INTRACELLULAR SODIUM VOLUME FRACTION; LIMIT OF QUANTITATION; MAGNETIC FIELD; MOLECULAR IMAGING; NON INVASIVE PROCEDURE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; SIGNAL NOISE RATIO; SINGLE QUANTUM FILTERED IMAGING; SODIUM CELL LEVEL; TISSUE SODIUM CONCENTRATION; TRIPLE QUANTUM FILTERED IMAGING;

ADULT; AGED; ALGORITHMS; BRAIN; COMPUTER SIMULATION; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MODELS, BIOLOGICAL; SODIUM; TISSUE DISTRIBUTION;

EID: 84871686027     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.2813     Document Type: Article

References (66)

1. Koch KS, Leffert HL. Increased sodium ion influx is necessary to initiate rat hepatocyte proliferation. Cell 1979; 18(1): 153-163.
2. Annunziato L, Pignataro G, Di Renzo GF. Pharmacology of brain Na+/Ca2+ exchanger: from molecular biology to therapeutic perspectives. Pharmacol. Rev. 2004; 56(4): 633-654.
3. Skou JC. The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochim. Biophys. Acta 1957; 23(2): 394-401.
4. Walker HK, Hall WD, Hurst JW. Clinical methods : the history, physical, and laboratory examinations. Boston: Butterworths; 1990. xxxi, pp. 1087.
5. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 1952; 117(4): 500-544.
6. Lang F. Mechanisms and significance of cell volume regulation. J. Am. Coll. Nutr. 2007; 26(5 Suppl): 613S-623S.
7. Jain RK. Transport of molecules in the tumor interstitium: a review. Cancer Res. 1987; 47(12): 3039-3051.
8. Cameron IL, Smith NK, Pool TB, Sparks RL. Intracellular concentration of sodium and other elements as related to mitogenesis and oncogenesis in vivo. Cancer Res. 1980; 40(5): 1493-1500.
9. Nagy I, Lustyik G, Lukacs G, Nagy V, Balazs G. Correlation of malignancy with the intracellular Na+:K+ratio in human thyroid tumors. Cancer Res. 1983; 43(11): 5395-5402.
10. Inglese M, Madelin G, Oesingmann N, Babb JS, Wu W, Stoeckel B, Herbert J, Johnson G. Brain tissue sodium concentration in multiple sclerosis: a sodium imaging study at 3 tesla. Brain 2010; 133(Pt 3): 847-857.
11. Thulborn KR, Davis D, Adams H, Gindin T, Zhou J. Quantitative tissue sodium concentration mapping of the growth of focal cerebral tumors with sodium magnetic resonance imaging. Magn. Reson. Med. 1999; 41(2): 351-359.
12. Christensen JD, Barrere BJ, Boada FE, Vevea JM, Thulborn KR. Quantitative tissue sodium concentration mapping of normal rat brain. Magn. Reson. Med. 1996; 36(1): 83-89.
13. Thulborn KR, Davis D, Snyder J, Yonas H, Kassam A. Sodium MR imaging of acute and subacute stroke for assessment of tissue viability. Neuroimaging Clin. N. Am. 2005; 15(3): 639-653, xi-xii.
14. Navon G, Shinar H, Eliav U, Seo Y. Multiquantum filters and order in tissues. NMR Biomed. 2001; 14(2): 112-132.
15. Winter PM, Seshan V, Makos JD, Sherry AD, Malloy CR, Bansal N. Quantitation of intracellular [Na+] in vivo by using TmDOTP5- as an NMR shift reagent and extracellular marker. J. Appl. Physiol. 1998; 85(5): 1806-1812.
16. Hutchison RB, Shapiro JI. Measurement of intracellular sodium with NMR methods. Concepts in Magnetic Resonance 1991; 3(4): 215-236.
17. Preston E, Foster DO. Diffusion into rat brain of contrast and shift reagents for magnetic resonance imaging and spectroscopy. NMR Biomed. 1993; 6(5): 339-344.
18. van der Veen JW, van Gelderen P, Creyghton JH, Bovee WM. Diffusion in red blood cell suspensions: separation of the intracellular and extracellular NMR sodium signal. Magn. Reson. Med. 1993; 29(4): 571-574.
19. Pekar J, Leigh J. Detection of biexponential relaxation in sodium-23 facilitated by double-quantum filtering. J. Magn. Reson. 1986; 69: 582-584.
20. Pekar J, Renshaw P, Leigh JS. Selective Detection of Intracellular Sodium by Coherence-Transfer NMR. J. Magn. Reson. 1987; 72: 159-161.
21. Nicholson C, Sykova E. Extracellular space structure revealed by diffusion analysis. Trends Neurosci. 1998; 21(5): 207-215.
22. Muller N, Bodenhausen G, Ernst RR. Relaxation-Induced Violations of Coherence Transfer Selection Rules in Nuclear Magnetic Resonance. J. Magn. Reson. 1987; 75: 297-334.
23. Borthakur A, Mellon E, Niyogi S, Witschey W, Kneeland JB, Reddy R. Sodium and T1rho MRI for molecular and diagnostic imaging of articular cartilage. NMR Biomed. 2006; 19(7): 781-821.
24. Hancu I, Boada FE, Shen GX. Three-dimensional triple-quantum-filtered (23)Na imaging of in vivo human brain. Magn. Reson. Med. 1999; 42(6): 1146-1154.
25. Kalyanapuram R, Seshan V, Bansal N. Three-dimensional triple-quantum-filtered 23Na imaging of the dog head in vivo. J. Magn. Reson. Imaging 1998; 8(5): 1182-1189.
26. Reddy R, Insko EK, Leigh JS. Triple quantum sodium imaging of articular cartilage. Magn. Reson. Med. 1997; 38(2): 279-284.
27. Borthakur A, Hancu I, Boada FE, Shen GX, Shapiro EM, Reddy R. In vivo triple quantum filtered twisted projection sodium MRI of human articular cartilage. J. Magn. Reson. 1999; 141(2): 286-290.
28. Schoeniger JS, Aiken N, Hsu E, Blackband SJ. Relaxation-time and diffusion NMR microscopy of single neurons. J. Magn. Reson. B 1994; 103(3): 261-273.
29. Grant SC, Buckley DL, Gibbs S, Webb AG, Blackband SJ. MR microscopy of multicomponent diffusion in single neurons. Magn. Reson. Med. 2001; 46(6): 1107-1112.
30. 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. 1986; 85: 6282.
31. Ouwerkerk R, Bleich KB, Gillen JS, Pomper MG, Bottomley PA. Tissue sodium concentration in human brain tumors as measured with 23Na MR imaging. Radiology 2003; 227(2): 529-537.
32. Thulborn KR, Ackerman JJH. Absolute molar concentrations by nmr in inhomogeneous B1. A scheme for analysis of in vivo metabolites. J. Magn. Reson. 1983; 55: 357-371.
33. Winter PM, Bansal N. Triple-quantum-filtered (23)Na NMR spectroscopy of subcutaneously implanted 9l gliosarcoma in the rat in the presence of TmDOTP(5-1). J. Magn. Reson. 2001; 152(1): 70-78.
34. Babs'kyi AM, Ju S, Topper S, Bennett S, Atthe B, McLennan G, Bansal N. Noninvasive monitoring of the hepatocellular carcinoma growth by the method of 1H and 23Na nuclear magnetic resonance. Ukr. Biokhim. Zh. 2008; 80(4): 130-137.
35. Tanase C, Boada FE. Triple-quantum-filtered imaging of sodium in presence of B(0) inhomogeneities. J. Magn. Reson. 2005; 174(2): 270-278.
36. Fleysher L, Oesingmann N, Inglese M. B0 inhomogeneity-insensitive triple-quantum-filtered sodium imaging using a 12-step phase-cycling scheme. NMR Biomed. 2010; 23(10): 1191-1198.
37. Kemp-Harper R, Styles P, Wimperis S. Measurement of 23Na transverse relaxation in vivo. The flip-angle-independent experiment. J. Magn. Reson. Series B. 1995; 109: 223-228.
38. Matthies C, Nagel AM, Schad LR, Bachert P. Reduction of B(0) inhomogeneity effects in triple-quantum-filtered sodium imaging. J. Magn. Reson. 2010; 202(2): 239-244.
39. Lu A, Atkinson IC, Claiborne TC, Damen FC, Thulborn KR. Quantitative sodium imaging with a flexible twisted projection pulse sequence. Magn. Reson. Med. 2010; 63(6): 1583-1593.
40. Schain RJ. Cerebrospinal fluid and serum cation levels. Arch. Neurol. 1964; 11: 330-333.
41. Cooper ES, Lechner E, Bellet S. Relation between serum and cerebrospinal fluid electrolytes under normal and abnormal conditions. Am. J. Med. 1955; 18(4): 613-621.
42. Tropp J. Reciprocity and gyrotropism in magnetic resonance transduction. Phys. Rev. A 2006; 74: 062103.
43. Hoult DI. The principle of reciprocity in signal strength calculations - a mathematical guide. Concepts in magnetic resonance. 2000; 124: 173-187.
44. Insko EK, Bolinger L. Mapping of the radiofrequency field. J. Magn. Reson. Series A. 1993; 103: 82-85.
45. Hancu I, van der Maarel JR, Boada FE. A model for the dynamics of spins 3/2 in biological media: signal loss during radiofrequency excitation in triple-quantum-filtered sodium MRI. J. Magn. Reson. 2000; 147(2): 179-191.
46. 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.
47. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004; 23(1): S208-219.
48. Bartha R, Menon RS. Long component time constant of 23Na T*2 relaxation in healthy human brain. Magn. Reson. Med. 2004; 52(2): 407-410.
49. Perman WH, Turski PA, Houston LW, Glover GH, Hayes CE. Methodology of in vivo human sodium MR imaging at 1.5 T. Radiology 1986; 160(3): 811-820.
50. Winkler SS, Thomasson DM, Sherwood K, Perman WH. Regional T2 and sodium concentration estimates in the normal human brain by sodium-23 MR imaging at 1.5 T. J. Comput. Assist. Tomogr. 1989; 13(4): 561-566.
51. Fleysher L, Oesingmann N, Stoeckel B, Grossman RI, Inglese M. Sodium long-component T(2)(*) mapping in human brain at 7 Tesla. Magn. Reson. Med. 2009; 62(5): 1338-1341.
52. Zaaraoui W, Fleysher L, Fleysher R, Liu S, Soher BJ, Gonen O. Human brain-structure resolved T(2) relaxation times of proton metabolites at 3 Tesla. Magn. Reson. Med. 2007; 57(6): 983-989.
53. Bevington PR, Robinson DK. Data reduction and error analysis for the physical sciences. Boston: McGraw-Hill; 2003. xi, pp. 320.
54. Pelligrino DA, Musch TI, Dempsey JA. Interregional differences in brain intracellular pH and water compartmentation during acute normoxic and hypoxic hypocapnia in the anesthetized dog. Brain Res. 1981; 214(2): 387-404.
55. Woodward DL, Reed DJ, Woodbury DM. Extracellular space of rat cerebral cortex. Am. J. Physiol. 1967; 212(2): 367-370.
56. Hirano A, Kato T. The Neuronal microenvironment. In: Boulton AA, Baker GB, Walz W (eds). Neuromethods. Volume 9. Clifton: Humana Press; 1988, p 105.
57. Sykova E, Nicholson C. Diffusion in brain extracellular space. Physiol. Rev. 2008; 88(4): 1277-1340.
58. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001; 14(1 Pt 1): 21-36.
59. Jernigan TL, Archibald SL, Fennema-Notestine C, Gamst AC, Stout JC, Bonner J, Hesselink JR. Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol. Aging 2001; 22(4): 581-594.
60. Eilers PH, Goeman JJ. Enhancing scatterplots with smoothed densities. Bioinformatics 2004; 20(5): 623-628.
61. Handel IG, Staddon GE, Weaver BMQ, Pearson MRB, Cruz-Madorran JI. Changes in packed cell volume during anaesthesia. Vet. Anaesth. Analg. 1991; 18: 347-352.
62. Atkinson IC, Lu A, Thulborn KR. Clinically constrained optimization of flexTPI acquisition parameters for the tissue sodium concentration bioscale. Magn. Reson. Med. 2011.
63. Goldsmith M, Damadian R. NMR in cancer. VII. Sodium-23 magnetic resonance of normal and cancerous tissues. Physiol. Chem. Phys. 1975; 7(3): 263-269.
64. Boada FE, Gillen JS, Shen GX, Chang SY, Thulborn KR. Fast three dimensional sodium imaging. Magn. Reson. Med. 1997; 37(5): 706-715.
65. Gurney PT, Hargreaves BA, Nishimura DG. Design and analysis of a practical 3D cones trajectory. Magn. Reson. Med. 2006; 55(3): 575-582.
66. Qian Y, Boada FE. Acquisition-weighted stack of spirals for fast high-resolution three-dimensional ultra-short echo time MR imaging. Magn. Reson. Med. 2008; 60(1): 135-145.