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  • Print publication year: 2013
  • Online publication date: January 2013

21 - Hyperpolarized Nuclear Magnetic Resonance Spectroscopy: A New Method for Metabolomic Research

from Section 4 - Metabolomic Nuclear Magnetic Resonance Spectroscopy Techniques for Body Tissue Analysis

References

1. Hoult, D.I., et al., Observation of tissue metabolites using 31P nuclear magnetic resonance. Nature, 1974. 252(5481):285–7.
2. Frahm, J., et al., Localized high-resolution proton NMR spectroscopy using stimulated echoes: initial applications to human brain in vivo. Magn Reson Med, 1989. 9(1):79–93.
3. Bottomley, P.A., Spatial localization in NMR spectroscopy in vivo. Ann N Y Acad Sci, 1987. 508:333–48.
4. Shulman, R.G., et al., Cellular applications of 31P and 13C nuclear magnetic resonance. Science, 1979. 205(4402):160–6.
5. Bowers, C.R. and D.P. Weitekamp, Transformation of symmetrization order to nuclear-spin magnetization by chemical reaction and nuclear magnetic resonance. Phys Rev Lett, 1986. 57(21):2645–8.
6. Bowers, C.R., Sensitivity enhancement utilizing parahydrogen. In Grand DM, Harris RK, editors. Encyclopedia of NMR, Hoboken, NJ: Wiley. 2002:750–69.
7. Kuhn, L.T., Transfer of parahydrogen-induced hyperpolarization to heteronuclei. Top Curr Chem, 2007. 276:25–68.
8. Adams, R.W., et al., Reversible interactions with para-hydrogen enhance NMR sensitivity by polarization transfer. Science, 2009. 323(5922):1708–11.
9. Overhauser, A.W., Polarization of nuclei in metals. Phys Rev, 1953. 92(2):411–5.
10. Carver, T.R. and C.P. Slichter, Polarization of nuclear spins in metals. Phys Rev, 1953. 92:212–3.
11. Abragam, A., Overhauser effect in nonmetals. Phys Rev, 1955. 98(6):1729–35.
12. Jeffries, C.D., Dynamic orientation of nuclei by forbidden transitions in paramagnetic resonance. Phys Rev, 1960. 117(4):1056–69.
13. de Boer, W., Borghini, M., Morimoto, K., Niinikoski, T. O., and Udo, F., Dynamic polarization of protons, deuterons, and carbon-13 nuclei: thermal contact between nuclear spins and an electron spin-spin interaction reservoir. J Low Temp Phys, 1974. 15(3/4):249–66.
14. Ardenkjaer-Larsen, J.H., et al., Increase in signal-to-noise ratio of >10,000 times in liquid-state. NMR. Proc Natl Acad Sci U S A 2003. 100(18):10158–63.
15. Albers, M.J., et al., Hyperpolarized 13C lactate, pyruvate, and alanine: noninvasive biomarkers for prostate cancer detection and grading. Cancer Res, 2008. 68(20):8607–15.
16. Day, S.E., et al., Detecting tumor response to treatment using hyperpolarized 13C magnetic resonance imaging and spectroscopy. Nat Med, 2007. 13(11):1382–7.
17. Golman, K., et al., Cardiac metabolism measured noninvasively by hyperpolarized 13C MRI. Magn Reson Med, 2008. 59(5):1005–13.
18. Hurd, R.E., et al., Cerebral dynamics and metabolism of hyperpolarized [1-(13)C]pyruvate using time-resolved MR spectroscopic imaging. J Cereb Blood Flow Metab, 2010. 30(10):1734–41.
19. Nelson, S.J., et al. Proof of concept clinical trial of hyperpolarized C-13 pyruvate in patients with prostate cancer. In ISMRM Annual Meeting, Melbourne, Australia, 2012.
20. Golman, K., et al., Overhauser-enhanced MR imaging (OMRI). Acta Radiol, 1998. 39(1):10–7.
21. Ardenkjaer-Larsen, J.H., Macholl, S., Johannesson, H., Dynamic nuclear polarization with trityls at 1.2K. Appl Magn Reson, 2008. 34:509–22.
22. Schroeder, M.A., et al., Real-time assessment of Krebs cycle metabolism using hyperpolarized 13C magnetic resonance spectroscopy. FASEB J, 2009. 23(8):2529–38.
23. Chen, A.P., et al. In vivo dynamic cardiac magnetic resonance spectroscopy with hyperpolarized [2–13C] pyruvate in pigs. In ISMRM Annual Meeting, Stockholm, Sweden, 2010.
24. Jensen, P.R., et al., Hyperpolarized amino acids for in vivo assays of transaminase activity. Chemistry, 2009. 15(39):10010–2.
25. Wilson, D.M., et al., Multi-compound polarization by DNP allows simultaneous assessment of multiple enzymatic activities in vivo. J Magn Reson, 2010. 205(1):141–7.
26. Zierhut, M.L., et al., Kinetic modeling of hyperpolarized 13C1-pyruvate metabolism in normal rats and TRAMP mice. J Magn Reson, 2010. 202(1):85–92.
27. Schulte, R.F., et al., Saturation-recovery metabolic imaging of hyperpolarised 13C pyruvate. In ISMRM Annual Meeting, Stockholm, Sweden, 2010.
28. Xu, T., et al., Quantitation of in vivo metabolic kinetics of pyruvate in rat kidneys in a single shot using hyperpolarized 13C magnetic resonance spectroscopic imaging. NMR in Biomedicine, 2011. 24(8):997–1005.
29. Romijn, J.A., et al., Lactate-pyruvate interconversion in blood: implications for in vivo tracer studies. Am J Physiol, 1994. 266(3 Pt 1):E334–40.
30. Kettunen, M.I., et al., Magnetization transfer measurements of exchange between hyperpolarized [1–13C]pyruvate and [1–13C]lactate in a murine lymphoma. Magn Reson Med, 2010. 63(4):872–80.
31. Spielman, D.M., et al., In vivo measurement of ethanol metabolism in the rat liver using magnetic resonance spectroscopy of hyperpolarized [1–13C]pyruvate. Magn Reson Med, 2009. 62(2):307–13.
32. Moreno, K.X., et al. Malate-aspartate shuttle reversal allows for lactate concentration increases upon rapid changes in 13C pyruvate concentration. In ISMRM Annual Meeting, Stockholm, Sweden, 2010.
33. Wilson, D.M., et al., Generation of hyperpolarized substrates by secondary labeling with [1,1–13C] acetic anhydride. Proc Natl Acad Sci U S A, 2009. 106(14):5503–7.
34. Hurd, R.E., et al., Metabolic imaging in the anesthetized rat brain using hyperpolarized [1–13C] pyruvate and [1–13C] ethyl pyruvate. Magn Reson Med, 2010. 63(5):1137–43.
35. Marjanska, M., et al., In vivo 13C spectroscopy in the rat brain using hyperpolarized [1-(13)C]pyruvate and [2-(13)C]pyruvate. J Magn Reson, 2010. 206(2):210–8.
36. Park, I., et al., Hyperpolarized 13C magnetic resonance metabolic imaging: application to brain tumors. Neuro Oncol, 2010. 12(2):133–44.
37. Witney, T.H., et al., Detecting treatment response in a model of human breast adenocarcinoma using hyperpolarised [1–13C]pyruvate and [1,4–13C2]fumarate. Br J Cancer, 2010. 103(9):1400–6.
38. Auricchio, A., et al., In vivo detection of gene expression in liver by 31P nuclear magnetic resonance spectroscopy employing creatine kinase as a marker gene. Proc Natl Acad Sci U S A, 2001. 98(9):5205–10.
39. Cui, W., et al., Novel NMR approach to assessing gene transfection: 4-fluoro-2-nitrophenyl-beta-D-galactopyranoside as a prototype reporter molecule for beta-galactosidase. Magn Reson Med, 2004. 51(3):616–20.
40. Chen, A.P., et al., 13C MR reporter probe system using dynamic nuclear polarization. NMR in Biomedicine, 2010. 24(5):514–20.
41. Jamin, Y., et al., Hyperpolarized (13)C magnetic resonance detection of carboxypeptidase G2 activity. Magn Reson Med, 2009. 62(5):1300–4.
42. Golman, K., R. in ‘t Zandt, M. Thaning, Real-time metabolic imaging. Proc Natl Acad Sci U S A, 2006. 103(30):11270–5.
43. Golman, K., et al., Metabolic imaging by hyperpolarized 13C magnetic resonance imaging for in vivo tumor diagnosis. Cancer Res, 2006. 66(22):10855–60.
44. Chen, A.P., et al., Hyperpolarized C-13 spectroscopic imaging of the TRAMP mouse at 3T-initial experience. Magn Reson Med, 2007. 58(6):1099–106.
45. Cunningham, C.H., et al., Double spin-echo sequence for rapid spectroscopic imaging of hyperpolarized 13C. J Magn Reson, 2007. 187(2):357–62.
46. Yen, Y.F., et al., Imaging considerations for in vivo 13C metabolic mapping using hyperpolarized 13C-pyruvate. Magn Reson Med, 2009. 62(1):1–10.
47. Mayer, D., et al., Fast metabolic imaging of systems with sparse spectra: application for hyperpolarized 13C imaging. Magn Reson Med, 2006. 56(4):932–7.
48. Levin, Y.S., et al., Optimization of fast spiral chemical shift imaging using least squares reconstruction: application for hyperpolarized (13)C metabolic imaging. Magn Reson Med, 2007. 58(2):245–52.
49. Mayer, D., et al., In vivo application of sub-second spiral chemical shift imaging (CSI) to hyperpolarized 13C metabolic imaging: comparison with phase-encoded CSI. J Magn Reson, 2010. 204(2):340–5.
50. Hurd, R.E., et al., Cerebral dynamics and metabolism of hyperpolarized [1-(13)C]pyruvate using time-resolved MR spectroscopic imaging. J Cereb Blood Flow Metab, 2010. 30(10):1734–41.
51. Mayer, D., et al., Application of subsecond spiral chemical shift imaging to real-time multislice metabolic imaging of the rat in vivo after injection of hyperpolarized 13C1-pyruvate. Magn Reson Med, 2009. 62(3):557–64.
52. Lustig, M., D. Donoho, and J.M. Pauly, Sparse MRI: the application of compressed sensing for rapid MR imaging. Magn Reson Med, 2007. 58(6):1182–95.
53. Hu, S., et al., Compressed sensing for resolution enhancement of hyperpolarized 13C flyback 3D-MRSI. J Magn Reson, 2008. 192(2):258–64.
54. Hu, S., et al., 3D compressed sensing for highly accelerated hyperpolarized (13)C MRSI with in vivo applications to transgenic mouse models of cancer. Magn Reson Med, 2010. 63(2):312–21.
55. Wiesinger, F., et al. Minimum-norm IDEAL spiral CSI for efficient hyperpolarized 13C metabolic imaging. In ISMRM Annual Meeting, Stockholm, Sweden, 2010.
56. Reeder, S.B., et al., Iterative decomposition of water and fat with echo asymmetry and least-squares estimation (IDEAL): application with fast spin-echo imaging. Magn Reson Med, 2005. 54(3):636–44.
57. Reeder, S.B., et al., Least-squares chemical shift separation for (13)C metabolic imaging. J Magn Reson Imaging, 2007. 26(4):1145–52.
58. Wiesinger, F., et al. Metabolic rate constant mapping of hyperpolarized 13C pyruvate. In ISMRM Annual Meeting, Stockholm, Sweden, 2010.
59. Darpolor, M.M., et al., In vivo magnetic resonance spectroscopic imaging of hyperpolarized [1–13C]-pyruvate metabolism in rat hepatocellular carcinoma. NMR Biomedicine, 2010. 24(5):506–13.
60. Josan, S., et al. Double spin-echo spiral chemical shift imaging for rapid metabolic imaging of hyperpolarized [1–13C]-pyruvate. In ISMRM Annual Meeting, Stockholm, Sweden, 2010.
61. Larson, P.E., et al., Multiband excitation pulses for hyperpolarized 13C dynamic chemical-shift imaging. J Magn Reson, 2008. 194(1):121–7.
62. Larson, P.E., et al., Fast dynamic 3D MR spectroscopic imaging with compressed sensing and multiband excitation pulses for hyperpolarized (13)C studies. Magn Reson Med, 2010. 65(3):610–9.
63. Larson, P.E., et al., Investigation of tumor hyperpolarized [1–13C]-pyruvate dynamics using time-resolved multiband RF excitation echo-planar MRSI. Magn Reson Med, 2010. 63(3):582–91.
64. Cunningham, C.H., et al., Pulse sequence for dynamic volumetric imaging of hyperpolarized metabolic products. J Magn Reson, 2008. 193(1):139–46.
65. Lau, A.Z., et al., Rapid multislice imaging of hyperpolarized (13)C pyruvate and bicarbonate in the heart. Magn Reson Med, 2010. 64(5):1323–31.
66. Yen, Y.F., et al., T(2) relaxation times of (13)C metabolites in a rat hepatocellular carcinoma model measured in vivo using (13)C-MRS of hyperpolarized [1-(13)C]pyruvate. NMR Biomed, 2010. 23(4):414–23.
67. Leupold, J., et al., Fast multiecho balanced SSFP metabolite mapping of (1)H and hyperpolarized (13)C compounds. MAGMA, 2009. 22(4):251–6.
68. Leupold, J., et al., Fast chemical shift mapping with multiecho balanced SSFP. MAGMA, 2006. 19(5):267–73.
69. Yen, Y.-F., et al. Signal enhancement in low-dose hyperpolarized 13C imaging using multi-slice FSEPSI sequence. In ISMRM Annual Meeting, Toronto, Canada, 2008.
70. Le Roux, P., Non-CPMG fast spin echo with full signal. J Magn Reson, 2002. 155(2):278–92.
71. Bastin, M.E. and P. Le Roux, On the application of a non-CPMG single-shot fast spin-echo sequence to diffusion tensor MRI of the human brain. Magn Reson Med, 2002. 48(1):6–14.
72. Yen, Y.-F., et al. Exploring multi-shot non-CPMG for hyperpolarized 13C metabolic MR spectroscopic imaging. In ISMRM Annual Meeting, Stockholm, Sweden, 2010.
73. Xu, T., et al. Quantitation of in-vivo metabolic kinetics of pyruvate using hyperpolarized 13C MRSI. In ISMRM Annual Meeting, Stockholm, Sweden, 2010.
74. Larson, P.E., et al., Generating super stimulated-echoes in MRI and their application to hyperpolarized C-13 diffusion metabolic imaging. IEEE Trans Med Imaging, 2012. 32(2):265–75.
75. Chekmenev, E.Y., et al., Hyperpolarized (1)H NMR employing low gamma nucleus for spin polarization storage. J Am Chem Soc, 2009. 131(9):3164–5.
76. Morris, G.A. and R. Freeman, Enhancement of nuclear magnetic resonance signals by polarization transfer. J Am Chem Soc, 1979. 101(3):760–2.
77. Sarkar, R., et al., Proton NMR of (15)N-choline metabolites enhanced by dynamic nuclear polarization. J Am Chem Soc, 2009. 131(44):16014–5.
78. Pfeilsticker, J.A., et al., A selective 15N-to-(1)H polarization transfer sequence for more sensitive detection of 15N-choline. J Magn Reson, 2010. 205(1):125–9.
79. Harris, T., P. Giraudeau, L. Frydman, Kinetics from indirectly detected hyperpolarized NMR spectroscopy by using spatially selective coherence transfers. Chemistry, 2010. 17(2):697–703.
80. Golman, K., et al., Molecular imaging with endogenous substances. Proc Natl Acad Sci U S A, 2003. 100(18):10435–9.
81. Kohler, S.J., et al., In vivo 13 carbon metabolic imaging at 3T with hyperpolarized 13C-1-pyruvate. Magn Reson Med, 2007. 58(1):65–9.
82. Chen, A., et al., In vivo hyperpolarized 13C MR spectroscopic imaging with 1H decoupling. J Magn Reson, 2009. 197(1):100–6.
83. Warren, W., et al., Increasing hyperpolarized spin lifetimes through true singlet eigenstates. Science, 2009. 323(5922):1711–4.
84. Carravetta, M., O.G. Johannessen, and M.H. Levitt, Beyond the T1 limit: singlet nuclear spin states in low magnetic fields. Phys Rev Lett, 2004. 92(15):153003.
85. Carravetta, M. and M.H. Levitt, Long-lived nuclear spin states in high-field solution NMR. J Am Chem Soc, 2004. 126(20):6228–9.
86. Sarkar, R., P.R. Vasos, G. Bodenhausen, Singlet-state exchange NMR spectroscopy for the study of very slow dynamic processes. J Am Chem Soc, 2007. 129(2):328–34.
87. Vasos, P.R., et al., Long-lived states to sustain hyperpolarized magnetization, in Proc Natl Acad Sci U S A, 2009. 106(44):18469–73.
88. Chen, A.P., et al., Feasibility of using hyperpolarized [1–13C]lactate as a substrate for in vivo metabolic 13C MRSI studies. Magn Reson Imaging, 2008. 26(6):721–6.
89. Gallagher, F.A., et al., Magnetic resonance imaging of pH in vivo using hyperpolarized 13C-labelled bicarbonate. Nature, 2008. 453(7197):940–3.
90. Gallagher, F.A., et al., Production of hyperpolarized [1,4–13C2]malate from [1,4–13C2]fumarate is a marker of cell necrosis and treatment response in tumors. Proc Natl Acad Sci U S A, 2009. 106(47):19801–6.
91. Keshari, K.R., et al., Hyperpolarized [2–13C]-fructose: a hemiketal DNP substrate for in vivo metabolic imaging. J Am Chem Soc, 2009. 131(48):17591–6.
92. Gallagher, F.A., et al., 13C MR spectroscopy measurements of glutaminase activity in human hepatocellular carcinoma cells using hyperpolarized 13C-labeled glutamine. Magn Reson Med, 2008. 60(2):253–7.
93. Jensen, P.R., et al., Detection of low-populated reaction intermediates with hyperpolarized NMR. Chem Commun (Camb), 2009(34):5168–70.
94. Johansson, E., et al., Cerebral perfusion assessment by bolus tracking using hyperpolarized 13C. Magn Reson Med, 2004. 51(3):464–72.
95. Karlsson, M., et al., Imaging of branched chain amino acid metabolism in tumors with hyperpolarized 13C ketoisocaproate. Int J Cancer, 2010. 127(3):729–36.
96. van Heeswijk, R.B., et al., Hyperpolarized lithium-6 as a sensor of nanomolar contrast agents. Magn Reson Med, 2009. 61(6):1489–93.
97. McCarney, E.R., et al., Hyperpolarized water as an authentic magnetic resonance imaging contrast agent. Proc Natl Acad Sci U S A, 2007. 104(6):1754–9.
98. Cudalbu, C., et al., Feasibility of in vivo 15N MRS detection of hyperpolarized 15N labeled choline in rats. Phys Chem Chem Phys, 2010. 12(22):5818–23.
99. Bhattacharya, P., et al., Towards hyperpolarized (13)C-succinate imaging of brain cancer. J Magn Reson, 2007. 186(1):150–5.
100. Merritt, M.E., et al., Hyperpolarized (89)Y offers the potential of direct imaging of metal ions in biological systems by magnetic resonance. J Am Chem Soc, 2007. 129(43):12942–3.