Skip to main content
Log in

13C imaging—a new diagnostic platform

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  1. Bloch F, Hansen WW, Packard M (1946) The nuclear induction experiment. Phys Rev 70:474–485

    Article  CAS  Google Scholar 

  2. Purcell EM, Torrey HC, Pound RV (1946) Resonance absorption by nuclear magnetic moments in a solid. Phys Rev 69:37–38

    Article  CAS  Google Scholar 

  3. Lauterbur PC (1973) Image formation by induced local interactions: examples employing nuclear magnetic resonance. Nature 242:190–191

    CAS  Google Scholar 

  4. Shulman RG, Rothman DL (2001) 13C NMR of intermediary metabolism: implications for systemic physiology. Annu Rev Physiol 63:15–48

    Article  CAS  PubMed  Google Scholar 

  5. Albert MS, Balamore D (1998) Development of hyperpolarized noble gas MRI. Nucl Instrum Methods Phys Res A 402:441–453

    CAS  PubMed  Google Scholar 

  6. 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 370:199–201

    Article  CAS  PubMed  Google Scholar 

  7. 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 33:271–275

    CAS  PubMed  Google Scholar 

  8. Kauczor H, Surkau R, Roberts T (1998) MRI using hyperpolarized noble gases. Eur Radiol 8:820–827

    CAS  PubMed  Google Scholar 

  9. Kauczor HU (2003) Hyperpolarized helium-3 gas magnetic resonance imaging of the lung. Top Magn Reson Imaging 14:223–230

    PubMed  Google Scholar 

  10. 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 20:540–554

    PubMed  Google Scholar 

  11. 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

    Google Scholar 

  12. 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 100:10158–10163

    CAS  PubMed  Google Scholar 

  13. 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 12:183–204

    CAS  PubMed  Google Scholar 

  14. 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. Frossati G (1998) Polarization of 3He, D2 (and possibly 129Xe) using cryogenic techniques. Nucl Instrum Meth A 402:479–483

    CAS  Google Scholar 

  16. Abragam A, Goldman M (1978) Principles of dynamic nuclear polarisation. Rep Prog Phys 41:395–467

    CAS  Google Scholar 

  17. Bowers CR, Weitekamp DP (1986) Transformation of symmetrization order to nuclear-spin magnetization by chemical reaction and nuclear magnetic resonance. Phys Rev Lett 57:2645–2648

    CAS  PubMed  Google Scholar 

  18. Bowers CR, Weitekamp DP (1987) Parahydrogen and synthesis allow dramatically enhanced nuclear alignment. J Am Chem Soc 109:5541–5542

    CAS  Google Scholar 

  19. Golman K, Axelsson O, Jóhannesson H, Månsson S, Olofsson C, Petersson JS (2001) Parahydrogen-induced polarization in imaging: subsecond 13C angiography. Magn Reson Med 46:1–5

    CAS  PubMed  Google Scholar 

  20. 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. 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

    Google Scholar 

  22. Merbach A, Tóth É (2001) The chemistry of contrast agents in medical magnetic resonance imaging. John Wiley & Sons, Chichester

    Google Scholar 

  23. Nishimura DG, Macovski A, Pauly JM (1986) Magnetic resonance angiography. IEEE Trans Med Imaging 5:140–151

    Google Scholar 

  24. Maki JH, Chenevert TL, Prince MR (1996) Three-dimensional contrast-enhanced MR angiography. Top Magn Reson Imaging 8:322–344

    CAS  PubMed  Google Scholar 

  25. Golman K, Ardenkjaer-Larsen JH, Petersson JS, Månsson S, Leunbach I (2003) Molecular imaging with endogenous substances. Proc Natl Acad Sci U S A 100:10435–10439

    CAS  PubMed  Google Scholar 

  26. 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–S510

    PubMed  Google Scholar 

  27. Markstaller K, Eberle B, Schreiber WG, Weiler N, Thelen M, Kauczor HU (2000) Flip angle considerations in (3)helium-MRI. NMR Biomed 13:190–193

    CAS  PubMed  Google Scholar 

  28. Zhao L, Albert MS (1998) Biomedical imaging using hyperpolarized noble gas MRI: pulse sequence considerations. Nucl Instrum Methods Phys Res A 402:454–460

    CAS  PubMed  Google Scholar 

  29. Svensson J, Månsson S, Johansson E, Petersson JS, Olsson LE (2003) Hyperpolarized 13C MR angiography using trueFISP. Magn Reson Med 50:256–262

    PubMed  Google Scholar 

  30. Kiselev VG (2001) On the theoretical basis of perfusion measurements by dynamic susceptibility contrast MRI. Magn Reson Med 46:1113–1122

    CAS  PubMed  Google Scholar 

  31. Larsson HB, Fritz-Hansen T, Rostrup E, Sondergaard L, Ring P, Henriksen O (1996) Myocardial perfusion modeling using MRI. Magn Reson Med 35:716–726

    CAS  PubMed  Google Scholar 

  32. 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 51:464–472

    CAS  PubMed  Google Scholar 

  33. Johansson E (2003) NMR imaging of flow and perfusion using hyperpolarized nuclei. Thesis, Lund University, Sweden

  34. 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. 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 52:1043–1051

    CAS  PubMed  Google Scholar 

  36. Uematsu H, Ohno Y, Hatabu H (2003) Recent advances in magnetic resonance perfusion imaging of the lung. Top Magn Reson Imaging 14:245–251

    PubMed  Google Scholar 

  37. 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

    Google Scholar 

  38. Kearon C (2003) Diagnosis of pulmonary embolism. CMAJ 168:183–194

    PubMed  Google Scholar 

  39. Wagner PD, Saltzman HA, West JB (1974) Measurement of continuous distributions of ventilation-perfusion ratios: theory. J Appl Physiol 36:588–599

    CAS  PubMed  Google Scholar 

  40. 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 82:943–953

    CAS  PubMed  Google Scholar 

  41. 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

    Google Scholar 

  42. 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

    CAS  Google Scholar 

  43. 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 84:709–716

    CAS  PubMed  Google Scholar 

  44. 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 49:216–222

    PubMed  Google Scholar 

  45. 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 12:590–594

    CAS  PubMed  Google Scholar 

  46. 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 21:404–410

    CAS  PubMed  Google Scholar 

  47. 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 8:1177–1181

    CAS  PubMed  Google Scholar 

  48. 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 202:273–276

    CAS  PubMed  Google Scholar 

  49. 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 16:104–109

    PubMed  Google Scholar 

  50. 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. Ross B, Michaelis T (1994) Clinical applications of magnetic resonance spectroscopy. Magn Reson Q 10:191–247

    CAS  PubMed  Google Scholar 

  52. Cousins JP (1995) Clinical MR spectroscopy: fundamentals, current applications, and future potential. Am J Roentgenol 164:1337–1347

    CAS  Google Scholar 

  53. Henriksen O (1994) MR spectroscopy in clinical research. Acta Radiol 35:96–116

    CAS  PubMed  Google Scholar 

  54. 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 15:579–590

    CAS  PubMed  Google Scholar 

  55. 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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sven Månsson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Månsson, S., Johansson, E., Magnusson, P. et al. 13C imaging—a new diagnostic platform. Eur Radiol 16, 57–67 (2006). https://doi.org/10.1007/s00330-005-2806-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-005-2806-x

Keywords

Navigation