Skip to main content
Top
Published in: European Radiology 1/2006

01-01-2006 | Magnetic Resonance

13C imaging—a new diagnostic platform

Authors: Sven Månsson, Edvin Johansson, Peter Magnusson, Chun-Ming Chai, Georg Hansson, J. Stefan Petersson, Freddy Ståhlberg, Klaes Golman

Published in: European Radiology | Issue 1/2006

Login to get access

Abstract

The evolution of magnetic resonance imaging (MRI) has been astounding since the early 1980s, and a broad range of applications has emerged. To date, clinical imaging of nuclei other than protons has been precluded for reasons of sensitivity. However, with the recent development of hyperpolarization techniques, the signal from a given number of nuclei can be increased as much as 100,000 times, sufficient to enable imaging of nonproton nuclei. Technically, imaging of hyperpolarized nuclei offers several unique properties, such as complete lack of background signal and possibility for local and permanent destruction of the signal by means of radio frequency (RF) pulses. These properties allow for improved as well as new techniques within several application areas. Diagnostically, the injected compounds can visualize information about flow, perfusion, excretory function, and metabolic status. In this review article, we explain the concept of hyperpolarization and the techniques to hyperpolarize 13C. An overview of results obtained within angiography, perfusion, and catheter tracking is given, together with a discussion of the particular advantages and limitations. Finally, possible future directions of hyperpolarized 13C MRI are pointed out.
Literature
1.
go back to reference Bloch F, Hansen WW, Packard M (1946) The nuclear induction experiment. Phys Rev 70:474–485CrossRef Bloch F, Hansen WW, Packard M (1946) The nuclear induction experiment. Phys Rev 70:474–485CrossRef
2.
go back to reference Purcell EM, Torrey HC, Pound RV (1946) Resonance absorption by nuclear magnetic moments in a solid. Phys Rev 69:37–38CrossRef Purcell EM, Torrey HC, Pound RV (1946) Resonance absorption by nuclear magnetic moments in a solid. Phys Rev 69:37–38CrossRef
3.
go back to reference Lauterbur PC (1973) Image formation by induced local interactions: examples employing nuclear magnetic resonance. Nature 242:190–191 Lauterbur PC (1973) Image formation by induced local interactions: examples employing nuclear magnetic resonance. Nature 242:190–191
4.
go back to reference Shulman RG, Rothman DL (2001) 13C NMR of intermediary metabolism: implications for systemic physiology. Annu Rev Physiol 63:15–48CrossRefPubMed Shulman RG, Rothman DL (2001) 13C NMR of intermediary metabolism: implications for systemic physiology. Annu Rev Physiol 63:15–48CrossRefPubMed
5.
go back to reference Albert MS, Balamore D (1998) Development of hyperpolarized noble gas MRI. Nucl Instrum Methods Phys Res A 402:441–453PubMed Albert MS, Balamore D (1998) Development of hyperpolarized noble gas MRI. Nucl Instrum Methods Phys Res A 402:441–453PubMed
6.
go back to reference Albert MS, Cates GD, Driehuys B, Happer W, Saam B, Springer CS Jr, Wishnia A (1994) Biological magnetic resonance imaging using laser-polarized 129Xe. Nature 370:199–201CrossRefPubMed Albert MS, Cates GD, Driehuys B, Happer W, Saam B, Springer CS Jr, Wishnia A (1994) Biological magnetic resonance imaging using laser-polarized 129Xe. Nature 370:199–201CrossRefPubMed
7.
go back to reference Middleton H, Black RD, Saam B, Cates GD, Cofer GP, Guenther R, Happer W, Hedlund LW, Johnson GA, Juvan K et al (1995) MR imaging with hyperpolarized 3He gas. Magn Reson Med 33:271–275PubMed Middleton H, Black RD, Saam B, Cates GD, Cofer GP, Guenther R, Happer W, Hedlund LW, Johnson GA, Juvan K et al (1995) MR imaging with hyperpolarized 3He gas. Magn Reson Med 33:271–275PubMed
8.
go back to reference Kauczor H, Surkau R, Roberts T (1998) MRI using hyperpolarized noble gases. Eur Radiol 8:820–827PubMed Kauczor H, Surkau R, Roberts T (1998) MRI using hyperpolarized noble gases. Eur Radiol 8:820–827PubMed
9.
go back to reference Kauczor HU (2003) Hyperpolarized helium-3 gas magnetic resonance imaging of the lung. Top Magn Reson Imaging 14:223–230PubMed Kauczor HU (2003) Hyperpolarized helium-3 gas magnetic resonance imaging of the lung. Top Magn Reson Imaging 14:223–230PubMed
10.
go back to reference van Beek EJ, Wild JM, Kauczor HU, Schreiber W, Mugler JP III, de Lange EE (2004) Functional MRI of the lung using hyperpolarized 3-helium gas. J Magn Reson Imaging 20:540–554PubMed van Beek EJ, Wild JM, Kauczor HU, Schreiber W, Mugler JP III, de Lange EE (2004) Functional MRI of the lung using hyperpolarized 3-helium gas. J Magn Reson Imaging 20:540–554PubMed
11.
go back to reference Jóhannesson H, Axelsson O, Karlsson M (2004) Transfer of para-hydrogen spin order into polarization by diabatic field cycling. C R Physique 5:315–324 Jóhannesson H, Axelsson O, Karlsson M (2004) Transfer of para-hydrogen spin order into polarization by diabatic field cycling. C R Physique 5:315–324
12.
go back to reference Ardenkjaer-Larsen JH, Fridlund B, Gram A, Hansson G, Hansson L, Lerche MH, Servin R, Thaning M, Golman K (2003) Increase in signal-to-noise ratio of >10,000 times in liquid-state NMR. Proc Natl Acad Sci U S A 100:10158–10163PubMed Ardenkjaer-Larsen JH, Fridlund B, Gram A, Hansson G, Hansson L, Lerche MH, Servin R, Thaning M, Golman K (2003) Increase in signal-to-noise ratio of >10,000 times in liquid-state NMR. Proc Natl Acad Sci U S A 100:10158–10163PubMed
13.
go back to reference Campeau NG, Huston J III, Bernstein MA, Lin C, Gibbs GF (2001) Magnetic resonance angiography at 3.0 Tesla: initial clinical experience. Top Magn Reson Imaging 12:183–204PubMed Campeau NG, Huston J III, Bernstein MA, Lin C, Gibbs GF (2001) Magnetic resonance angiography at 3.0 Tesla: initial clinical experience. Top Magn Reson Imaging 12:183–204PubMed
14.
go back to reference Ardenkjaer-Larsen JH, Axelsson O, Golman K, Wistrand LG, Hansson G, Leunbach I, Petersson JS (1999) Method of magnetic resonance investigation. International patent application no. WO 99/35508 Ardenkjaer-Larsen JH, Axelsson O, Golman K, Wistrand LG, Hansson G, Leunbach I, Petersson JS (1999) Method of magnetic resonance investigation. International patent application no. WO 99/35508
15.
go back to reference Frossati G (1998) Polarization of 3He, D2 (and possibly 129Xe) using cryogenic techniques. Nucl Instrum Meth A 402:479–483 Frossati G (1998) Polarization of 3He, D2 (and possibly 129Xe) using cryogenic techniques. Nucl Instrum Meth A 402:479–483
16.
go back to reference Abragam A, Goldman M (1978) Principles of dynamic nuclear polarisation. Rep Prog Phys 41:395–467 Abragam A, Goldman M (1978) Principles of dynamic nuclear polarisation. Rep Prog Phys 41:395–467
17.
go back to reference Bowers CR, Weitekamp DP (1986) Transformation of symmetrization order to nuclear-spin magnetization by chemical reaction and nuclear magnetic resonance. Phys Rev Lett 57:2645–2648PubMed Bowers CR, Weitekamp DP (1986) Transformation of symmetrization order to nuclear-spin magnetization by chemical reaction and nuclear magnetic resonance. Phys Rev Lett 57:2645–2648PubMed
18.
go back to reference Bowers CR, Weitekamp DP (1987) Parahydrogen and synthesis allow dramatically enhanced nuclear alignment. J Am Chem Soc 109:5541–5542 Bowers CR, Weitekamp DP (1987) Parahydrogen and synthesis allow dramatically enhanced nuclear alignment. J Am Chem Soc 109:5541–5542
19.
go back to reference Golman K, Axelsson O, Jóhannesson H, Månsson S, Olofsson C, Petersson JS (2001) Parahydrogen-induced polarization in imaging: subsecond 13C angiography. Magn Reson Med 46:1–5PubMed Golman K, Axelsson O, Jóhannesson H, Månsson S, Olofsson C, Petersson JS (2001) Parahydrogen-induced polarization in imaging: subsecond 13C angiography. Magn Reson Med 46:1–5PubMed
20.
go back to reference Jóhannesson H, Axelsson O, Karlsson M, Goldman M (2004) Methods to convert para-hydrogen spin order into hetero nuclei polarization for in vivo detection. In: Proc 21st Annual Meeting ESMRMB:144 Jóhannesson H, Axelsson O, Karlsson M, Goldman M (2004) Methods to convert para-hydrogen spin order into hetero nuclei polarization for in vivo detection. In: Proc 21st Annual Meeting ESMRMB:144
21.
go back to reference Prince MR, Yucel EK, Kaufman JA, Harrison DC, Geller SC (1993) Dynamic gadolinium-enhanced three-dimensional abdominal MR arteriography. J Magn Reson Imaging 3:877–881 Prince MR, Yucel EK, Kaufman JA, Harrison DC, Geller SC (1993) Dynamic gadolinium-enhanced three-dimensional abdominal MR arteriography. J Magn Reson Imaging 3:877–881
22.
go back to reference Merbach A, Tóth É (2001) The chemistry of contrast agents in medical magnetic resonance imaging. John Wiley & Sons, Chichester Merbach A, Tóth É (2001) The chemistry of contrast agents in medical magnetic resonance imaging. John Wiley & Sons, Chichester
23.
go back to reference Nishimura DG, Macovski A, Pauly JM (1986) Magnetic resonance angiography. IEEE Trans Med Imaging 5:140–151 Nishimura DG, Macovski A, Pauly JM (1986) Magnetic resonance angiography. IEEE Trans Med Imaging 5:140–151
24.
go back to reference Maki JH, Chenevert TL, Prince MR (1996) Three-dimensional contrast-enhanced MR angiography. Top Magn Reson Imaging 8:322–344PubMed Maki JH, Chenevert TL, Prince MR (1996) Three-dimensional contrast-enhanced MR angiography. Top Magn Reson Imaging 8:322–344PubMed
25.
go back to reference Golman K, Ardenkjaer-Larsen JH, Petersson JS, Månsson S, Leunbach I (2003) Molecular imaging with endogenous substances. Proc Natl Acad Sci U S A 100:10435–10439PubMed Golman K, Ardenkjaer-Larsen JH, Petersson JS, Månsson S, Leunbach I (2003) Molecular imaging with endogenous substances. Proc Natl Acad Sci U S A 100:10435–10439PubMed
26.
go back to reference Golman K, Ardenkjaer-Larsen JH, Svensson J, Axelsson O, Hansson G, Hansson L, Johannesson H, Leunbach I, Månsson S, Petersson JS, Pettersson G, Servin R, Wistrand LG (2002) 13C-angiography. Acad Radiol 9(Suppl 2):S507–S510PubMed Golman K, Ardenkjaer-Larsen JH, Svensson J, Axelsson O, Hansson G, Hansson L, Johannesson H, Leunbach I, Månsson S, Petersson JS, Pettersson G, Servin R, Wistrand LG (2002) 13C-angiography. Acad Radiol 9(Suppl 2):S507–S510PubMed
27.
go back to reference Markstaller K, Eberle B, Schreiber WG, Weiler N, Thelen M, Kauczor HU (2000) Flip angle considerations in (3)helium-MRI. NMR Biomed 13:190–193PubMed Markstaller K, Eberle B, Schreiber WG, Weiler N, Thelen M, Kauczor HU (2000) Flip angle considerations in (3)helium-MRI. NMR Biomed 13:190–193PubMed
28.
go back to reference Zhao L, Albert MS (1998) Biomedical imaging using hyperpolarized noble gas MRI: pulse sequence considerations. Nucl Instrum Methods Phys Res A 402:454–460PubMed Zhao L, Albert MS (1998) Biomedical imaging using hyperpolarized noble gas MRI: pulse sequence considerations. Nucl Instrum Methods Phys Res A 402:454–460PubMed
29.
go back to reference Svensson J, Månsson S, Johansson E, Petersson JS, Olsson LE (2003) Hyperpolarized 13C MR angiography using trueFISP. Magn Reson Med 50:256–262PubMed Svensson J, Månsson S, Johansson E, Petersson JS, Olsson LE (2003) Hyperpolarized 13C MR angiography using trueFISP. Magn Reson Med 50:256–262PubMed
30.
go back to reference Kiselev VG (2001) On the theoretical basis of perfusion measurements by dynamic susceptibility contrast MRI. Magn Reson Med 46:1113–1122PubMed Kiselev VG (2001) On the theoretical basis of perfusion measurements by dynamic susceptibility contrast MRI. Magn Reson Med 46:1113–1122PubMed
31.
go back to reference Larsson HB, Fritz-Hansen T, Rostrup E, Sondergaard L, Ring P, Henriksen O (1996) Myocardial perfusion modeling using MRI. Magn Reson Med 35:716–726PubMed Larsson HB, Fritz-Hansen T, Rostrup E, Sondergaard L, Ring P, Henriksen O (1996) Myocardial perfusion modeling using MRI. Magn Reson Med 35:716–726PubMed
32.
go back to reference Johansson E, Månsson S, Wirestam R, Svensson J, Petersson JS, Golman K, Ståhlberg F (2004) Cerebral perfusion assessment by bolus tracking using hyperpolarized 13C. Magn Reson Med 51:464–472PubMed Johansson E, Månsson S, Wirestam R, Svensson J, Petersson JS, Golman K, Ståhlberg F (2004) Cerebral perfusion assessment by bolus tracking using hyperpolarized 13C. Magn Reson Med 51:464–472PubMed
33.
go back to reference Johansson E (2003) NMR imaging of flow and perfusion using hyperpolarized nuclei. Thesis, Lund University, Sweden Johansson E (2003) NMR imaging of flow and perfusion using hyperpolarized nuclei. Thesis, Lund University, Sweden
34.
go back to reference Johansson E, Magnusson P, Chai C-M, Petersson J, Golman K, Wirestam R, Ståhlberg F (2004) Assessing myocardial perfusion using hyperpolarized 13C. In: Proc 21st Annual Meeting ESMRMB:117 Johansson E, Magnusson P, Chai C-M, Petersson J, Golman K, Wirestam R, Ståhlberg F (2004) Assessing myocardial perfusion using hyperpolarized 13C. In: Proc 21st Annual Meeting ESMRMB:117
35.
go back to reference Johansson E, Olsson LE, Mansson S, Petersson JS, Golman K, Ståhlberg F, Wirestam R (2004) Perfusion assessment with bolus differentiation: a technique applicable to hyperpolarized tracers. Magn Reson Med 52:1043–1051PubMed Johansson E, Olsson LE, Mansson S, Petersson JS, Golman K, Ståhlberg F, Wirestam R (2004) Perfusion assessment with bolus differentiation: a technique applicable to hyperpolarized tracers. Magn Reson Med 52:1043–1051PubMed
36.
go back to reference Uematsu H, Ohno Y, Hatabu H (2003) Recent advances in magnetic resonance perfusion imaging of the lung. Top Magn Reson Imaging 14:245–251PubMed Uematsu H, Ohno Y, Hatabu H (2003) Recent advances in magnetic resonance perfusion imaging of the lung. Top Magn Reson Imaging 14:245–251PubMed
37.
go back to reference West JB, Wagner PD (1997) Ventilation-perfusion relationships. In: Crystal RG, West JB, Barnes PJ, Weibel ER (eds) The lung: scientific foundations. Lippincott Williams & Wilkins, Philadelphia, pp 1693–1709 West JB, Wagner PD (1997) Ventilation-perfusion relationships. In: Crystal RG, West JB, Barnes PJ, Weibel ER (eds) The lung: scientific foundations. Lippincott Williams & Wilkins, Philadelphia, pp 1693–1709
38.
go back to reference Kearon C (2003) Diagnosis of pulmonary embolism. CMAJ 168:183–194PubMed Kearon C (2003) Diagnosis of pulmonary embolism. CMAJ 168:183–194PubMed
39.
go back to reference Wagner PD, Saltzman HA, West JB (1974) Measurement of continuous distributions of ventilation-perfusion ratios: theory. J Appl Physiol 36:588–599PubMed Wagner PD, Saltzman HA, West JB (1974) Measurement of continuous distributions of ventilation-perfusion ratios: theory. J Appl Physiol 36:588–599PubMed
40.
go back to reference Robertson HT, Glenny RW, Stanford D, McInnes LM, Luchtel DL, Covert D (1997) High-resolution maps of regional ventilation utilizing inhaled fluorescent microspheres. J Appl Physiol 82:943–953PubMed Robertson HT, Glenny RW, Stanford D, McInnes LM, Luchtel DL, Covert D (1997) High-resolution maps of regional ventilation utilizing inhaled fluorescent microspheres. J Appl Physiol 82:943–953PubMed
41.
go back to reference Edelman RR, Hatabu H, Tadamura E, Li W, Prasad PV (1996) Noninvasive assessment of regional ventilation in the human lung using oxygen-enhanced magnetic resonance imaging. Nat Med 2:1236–1239 Edelman RR, Hatabu H, Tadamura E, Li W, Prasad PV (1996) Noninvasive assessment of regional ventilation in the human lung using oxygen-enhanced magnetic resonance imaging. Nat Med 2:1236–1239
42.
go back to reference Ohno Y, Hatabu H, Takenaka D, Adachi S, Van Cauteren M, Sugimura K (2001) Oxygen-enhanced MR ventilation imaging of the lung: preliminary clinical experience in 25 subjects. Am J Roentgenol 177:185–194 Ohno Y, Hatabu H, Takenaka D, Adachi S, Van Cauteren M, Sugimura K (2001) Oxygen-enhanced MR ventilation imaging of the lung: preliminary clinical experience in 25 subjects. Am J Roentgenol 177:185–194
43.
go back to reference Simon BA, Marcucci C, Fung M, Lele SR (1998) Parameter estimation and confidence intervals for Xe-CT ventilation studies: a Monte Carlo approach. J Appl Physiol 84:709–716PubMed Simon BA, Marcucci C, Fung M, Lele SR (1998) Parameter estimation and confidence intervals for Xe-CT ventilation studies: a Monte Carlo approach. J Appl Physiol 84:709–716PubMed
44.
go back to reference Peters DC, Lederman RJ, Dick AJ, Raman VK, Guttman MA, Derbyshire JA, McVeigh ER (2003) Undersampled projection reconstruction for active catheter imaging with adaptable temporal resolution and catheter-only views. Magn Reson Med 49:216–222PubMed Peters DC, Lederman RJ, Dick AJ, Raman VK, Guttman MA, Derbyshire JA, McVeigh ER (2003) Undersampled projection reconstruction for active catheter imaging with adaptable temporal resolution and catheter-only views. Magn Reson Med 49:216–222PubMed
45.
go back to reference Serfaty JM, Yang X, Aksit P, Quick HH, Solaiyappan M, Atalar E (2000) Toward MRI-guided coronary catheterization: visualization of guiding catheters, guidewires, and anatomy in real time. J Magn Reson Imaging 12:590–594PubMed Serfaty JM, Yang X, Aksit P, Quick HH, Solaiyappan M, Atalar E (2000) Toward MRI-guided coronary catheterization: visualization of guiding catheters, guidewires, and anatomy in real time. J Magn Reson Imaging 12:590–594PubMed
46.
go back to reference Wildermuth S, Dumoulin CL, Pfammatter T, Maier SE, Hofmann E, Debatin JF (1998) MR-guided percutaneous angioplasty: assessment of tracking safety, catheter handling and functionality. Cardiovasc Intervent Radiol 21:404–410PubMed Wildermuth S, Dumoulin CL, Pfammatter T, Maier SE, Hofmann E, Debatin JF (1998) MR-guided percutaneous angioplasty: assessment of tracking safety, catheter handling and functionality. Cardiovasc Intervent Radiol 21:404–410PubMed
47.
go back to reference Zimmermann-Paul GG, Ladd ME, Pfammatter T, Hilfiker PR, Quick HH, Debatin JF (1998) MR versus fluoroscopic guidance of a catheter/guidewire system: in vitro comparison of steerability. J Magn Reson Imaging 8:1177–1181PubMed Zimmermann-Paul GG, Ladd ME, Pfammatter T, Hilfiker PR, Quick HH, Debatin JF (1998) MR versus fluoroscopic guidance of a catheter/guidewire system: in vitro comparison of steerability. J Magn Reson Imaging 8:1177–1181PubMed
48.
go back to reference Bakker CJ, Hoogeveen RM, Hurtak WF, van Vaals JJ, Viergever MA, Mali WP (1997) MR-guided endovascular interventions: susceptibility-based catheter and near-real-time imaging technique. Radiology 202:273–276PubMed Bakker CJ, Hoogeveen RM, Hurtak WF, van Vaals JJ, Viergever MA, Mali WP (1997) MR-guided endovascular interventions: susceptibility-based catheter and near-real-time imaging technique. Radiology 202:273–276PubMed
49.
go back to reference Green JD, Omary RA, Finn JP, Tang R, Li Y, Carr J, Li D (2002) Passive catheter tracking using MRI: comparison of conventional and magnetization-prepared FLASH. J Magn Reson Imaging 16:104–109PubMed Green JD, Omary RA, Finn JP, Tang R, Li Y, Carr J, Li D (2002) Passive catheter tracking using MRI: comparison of conventional and magnetization-prepared FLASH. J Magn Reson Imaging 16:104–109PubMed
50.
go back to reference Magnusson P, Månsson S, Petersson J, Chai C-M, Hansson G, Johansson E (2004) Passive catheter tracking using MRI and hyperpolarized 13C. In: Proc 21st Annual Meeting ESMRMB:143 Magnusson P, Månsson S, Petersson J, Chai C-M, Hansson G, Johansson E (2004) Passive catheter tracking using MRI and hyperpolarized 13C. In: Proc 21st Annual Meeting ESMRMB:143
51.
go back to reference Ross B, Michaelis T (1994) Clinical applications of magnetic resonance spectroscopy. Magn Reson Q 10:191–247PubMed Ross B, Michaelis T (1994) Clinical applications of magnetic resonance spectroscopy. Magn Reson Q 10:191–247PubMed
52.
go back to reference Cousins JP (1995) Clinical MR spectroscopy: fundamentals, current applications, and future potential. Am J Roentgenol 164:1337–1347 Cousins JP (1995) Clinical MR spectroscopy: fundamentals, current applications, and future potential. Am J Roentgenol 164:1337–1347
53.
go back to reference Henriksen O (1994) MR spectroscopy in clinical research. Acta Radiol 35:96–116PubMed Henriksen O (1994) MR spectroscopy in clinical research. Acta Radiol 35:96–116PubMed
54.
go back to reference Sonnewald U, Gribbestad IS, Westergaard N, Nilsen G, Unsgard G, Schousboe A, Petersen SB (1994) Nuclear magnetic resonance spectroscopy: biochemical evaluation of brain function in vivo and in vitro. Neurotoxicology 15:579–590PubMed Sonnewald U, Gribbestad IS, Westergaard N, Nilsen G, Unsgard G, Schousboe A, Petersen SB (1994) Nuclear magnetic resonance spectroscopy: biochemical evaluation of brain function in vivo and in vitro. Neurotoxicology 15:579–590PubMed
55.
go back to reference Kety SS, Schmidt CF (1948) The nitrous oxide method for the quantitative determination of cerebral blood flow in man: theory, procedure and normal values. J Clin Invest 27:476–483 Kety SS, Schmidt CF (1948) The nitrous oxide method for the quantitative determination of cerebral blood flow in man: theory, procedure and normal values. J Clin Invest 27:476–483
Metadata
Title
13C imaging—a new diagnostic platform
Authors
Sven Månsson
Edvin Johansson
Peter Magnusson
Chun-Ming Chai
Georg Hansson
J. Stefan Petersson
Freddy Ståhlberg
Klaes Golman
Publication date
01-01-2006
Publisher
Springer-Verlag
Published in
European Radiology / Issue 1/2006
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-005-2806-x

Other articles of this Issue 1/2006

European Radiology 1/2006 Go to the issue