Skip to main content
Log in

Minimizing the effects of magnetization transfer asymmetry on inhomogeneous magnetization transfer (ihMT) at ultra-high magnetic field (11.75 T)

  • Research Article
  • Published:
Magnetic Resonance Materials in Physics, Biology and Medicine Aims and scope Submit manuscript

Abstract

Objectives

The recently reported inhomogeneous magnetization transfer technique (ihMT) has been proposed for specific imaging of inhomogeneously broadened lines, and has shown great promise for characterizing myelinated tissues. The ihMT contrast is obtained by subtracting magnetization transfer images obtained with simultaneous saturation at positive and negative frequency offsets (dual frequency saturation experiment, MT +/) from those obtained with single frequency saturation (MT +) at the same total power. Hence, ihMT may be biased by MT-asymmetry, especially at ultra-high magnetic field. Use of the average of single positive and negative frequency offset saturation MT images, i.e., (MT ++MT ) has been proposed to correct the ihMT signal from MT-asymmetry signal.

Materials and methods

The efficiency of this correction method was experimentally assessed in this study, performed at 11.75 T on mice. Quantitative corrected ihMT and MT-asymmetry ratios (ihMTR and MTRasym) were measured in mouse brain structures for several MT-asymmetry magnitudes and different saturation parameter sets.

Results

Our results indicated a “safe” range of magnitudes (/MTRasym/<4 %) for which MT-asymmetry signal did not bias the corrected ihMT signal. Moreover, experimental evidence of the different natures of both MT-asymmetry and inhomogeneous MT contrasts were provided. In particular, non-zero ihMT ratios were obtained at zero MTRasym values.

Conclusion

MTRasym is not a confounding factor for ihMT quantification, even at ultra-high field, as long as MTRasym is restricted to ±4 %.

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

Similar content being viewed by others

References

  1. Yeung HN, Adler RS, Swanson SD (1994) Transient decay of longitudinal magnetization in heterogeneous spin systems under selective saturation. IV. Reformulation of the spin-bath-model equations by the redfield-provotorov theory. J Magn Reson A 106:37–45

    Article  CAS  Google Scholar 

  2. Morrison C, Stanisz G, Henkelman RM (1995) Modeling magnetization transfer for biological-like systems using a semi-solid pool with a super-Lorentzian lineshape and dipolar reservoir. J Magn Reson B 108:103–113

    Article  CAS  PubMed  Google Scholar 

  3. Morrison C, Mark Henkelman R (1995) A model for magnetization transfer in tissues. Magn Reson Med 33:475–482

    Article  CAS  PubMed  Google Scholar 

  4. Henkelman RM, Huang X, Xiang Q-S, Stanisz GJ, Swanson SD, Bronskill MJ (1993) Quantitative interpretation of magnetization transfer. Magn Reson Med 29:759–766

    Article  CAS  PubMed  Google Scholar 

  5. Sled JG, Pike GB (2001) Quantitative imaging of magnetization transfer exchange and relaxation properties in vivo using MRI. Magn Reson Med 46:923–931

    Article  CAS  PubMed  Google Scholar 

  6. Yarnykh VL, Yuan C (2004) Cross-relaxation imaging reveals detailed anatomy of white matter fiber tracts in the human brain. NeuroImage 23:409–424

    Article  PubMed  Google Scholar 

  7. Underhill HR, Rostomily RC, Mikheev AM, Yuan C, Yarnykh VL (2011) Fast bound pool fraction imaging of the in vivo rat brain: association with myelin content and validation in the C6 glioma model. NeuroImage 54:2052–2065

    Article  PubMed  Google Scholar 

  8. Samsonov A, Alexander AL, Mossahebi P, Wu Y-C, Duncan ID, Field AS (2012) Quantitative MR imaging of two-pool magnetization transfer model parameters in myelin mutant shaking pup. NeuroImage 62:1390–1398

    Article  PubMed  PubMed Central  Google Scholar 

  9. Schmierer K, Tozer DJ, Scaravilli F, Altmann DR, Barker GJ, Tofts PS, Miller DH (2007) Quantitative magnetization transfer imaging in postmortem multiple sclerosis brain. J Magn Reson Imaging JMRI 26:41–51

    Article  PubMed  Google Scholar 

  10. Tozer D, Ramani A, Barker GJ, Davies GR, Miller DH, Tofts PS (2003) Quantitative magnetization transfer mapping of bound protons in multiple sclerosis. Magn Reson Med 50:83–91

    Article  CAS  PubMed  Google Scholar 

  11. Davies GR, Ramani A, Dalton CM, Tozer DJ, Wheeler-Kingshott CAM, Barker GJ, Thompson AJ, Miller DH, Tofts PS (2003) Preliminary magnetic resonance study of the macromolecular proton fraction in white matter: a potential marker of myelin? Mult Scler Houndmills Basingstoke Engl 9:246–249

    Article  CAS  Google Scholar 

  12. Hua J, Jones CK, Blakeley J, Smith SA, van Zijl PCM, Zhou J (2007) Quantitative description of the asymmetry in magnetization transfer effects around the water resonance in the human brain. Magn Reson Med 58:786–793

    Article  PubMed  PubMed Central  Google Scholar 

  13. Pekar J, Jezzard P, Roberts DA, Leigh JS, Frank JA, McLaughlin AC (1996) Perfusion imaging with compensation for asymmetric magnetization transfer effects. Magn Reson Med 35:70–79

    Article  CAS  PubMed  Google Scholar 

  14. Swanson SD, Pang Y (2003) MT is symmetric but shifted with respect to water. Int Soc Magn Reson Med Toronto, Canada, p 660

  15. Jin T, Wang P, Zong X, Kim S-G (2012) Magnetic resonance imaging of the Amine-Proton EXchange (APEX) dependent contrast. NeuroImage 59:1218–1227

    Article  CAS  PubMed  Google Scholar 

  16. Jin T, Wang P, Zong X, Kim S-G (2013) MR imaging of the amide-proton transfer effect and the pH-insensitive nuclear overhauser effect at 9.4 T. Magn Reson Med 69:760–770

    Article  CAS  PubMed  Google Scholar 

  17. Varma G, Duhamel G, de Bazelaire C, Alsop DC (2015) Magnetization transfer from inhomogeneously broadened lines: a potential marker for myelin: magnetization transfer from inhomogeneously broadened lines. Magn Reson Med 73:614–622

    Article  CAS  PubMed  Google Scholar 

  18. Girard OM, Prevost VH, Varma G, Cozzone PJ, Alsop DC, Duhamel G (2015) Magnetization transfer from inhomogeneously broadened lines (ihMT): experimental optimization of saturation parameters for human brain imaging at 1.5 Tesla: Optimizing Saturation Parameters for ihMT Brain Imaging at 1.5 T. Magn Reson Med 73:2111–2121

    Article  PubMed  Google Scholar 

  19. Varma G, Girard OM, Prevost VH, Grant AK, Duhamel G, Alsop DC (2015) Interpretation of magnetization transfer from inhomogeneously broadened lines (ihMT) in tissues as a dipolar order effect within motion restricted molecules. J Magn Reson 260:67–76

    Article  CAS  PubMed  Google Scholar 

  20. Maricq MM, Waugh JS (1979) NMR in rotating solids. J Chem Phys 70:3300

    Article  CAS  Google Scholar 

  21. Davis JH, Auger M, Hodges RS (1995) High resolution 1H nuclear magnetic resonance of a transmembrane peptide. Biophys J 69:1917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Chen J-H, Sambol EB, DeCarolis P, O’Connor R, Geha RC, Wu YV, Singer S (2006) High-resolution MAS NMR spectroscopy detection of the spin magnetization exchange by cross-relaxation and chemical exchange in intact cell lines and human tissue specimens. Magn Reson Med 55:1246–1256

    Article  CAS  PubMed  Google Scholar 

  23. Huster D, Yao X, Hong M (2002) Membrane protein topology probed by (1)H spin diffusion from lipids using solid-state NMR spectroscopy. J Am Chem Soc 124:874–883

    Article  CAS  PubMed  Google Scholar 

  24. Horch RA, Gore JC, Does MD (2011) Origins of the ultrashort-T21H NMR signals in myelinated nerve: a direct measure of myelin content? Magn Reson Med 66:24–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Portis AM (1953) Electronic structure of F centers: saturation of the electron spin resonance. Phys Rev 91:1071

    Article  CAS  Google Scholar 

  26. Slichter CP (1990) Magnetic dipolar broadening of rigid lattices. In: Principles of magnetic resonance, Springer series in solid-state sciences, 3 edn, chap no 3. Springer, Berlin, p 65

  27. Scheidegger R, Vinogradov E, Alsop DC (2011) Amide proton transfer imaging with improved robustness to magnetic field inhomogeneity and magnetization transfer asymmetry using saturation with frequency alternating RF irradiation. Magn Reson Med 66:1275–1285

    Article  PubMed  PubMed Central  Google Scholar 

  28. Prevost VH, Girard OM, Varma G, Alsop DC, Duhamel G (2014) Magnetization transfer from inhomogeneoulsy broadened lines (ihMT): Qualitative Evaluation of ihMT Specificity toward Myelinated Structures. Int Soc Magn Reson Med, Milan, Italy, p 1498

  29. Jin T, Kim S-G (2014) Selection of irradiation parameters to minimize asymmetric magnetization transfer and NOE contributions in CEST. Int Soc Magn Reson Med Milan, Italy, p 3300

  30. Gruetter R (1993) Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn Reson Med 29:804–811

    Article  CAS  PubMed  Google Scholar 

  31. Ng M-C, Hua J, Hu Y, Luk KD, Lam EY (2009) Magnetization transfer (MT) asymmetry around the water resonance in human cervical spinal cord. J Magn Reson Imaging 29:523–528

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hua J, van Zijl PC, Sun PZ, Zhou J (2007) Quantitative description of magnetization transfer (MT) Asymmetry in experimental brain tumors. Int Soc Magn Reson Med, Berlin, Germany, p 882

  33. Varma G, Kourtelidis, F F, Alsop DC (2013) Quantitative Evaluation of the Exchange Time and T2 Associated with an inhomogeneous component using inhomogeneous magnetization transfer imaging. Int Soc Magn Reson Med Salt Lake City, Utah, USA, p 2536

  34. Zu Z, Janve VA, Xu J, Does MD, Gore JC, Gochberg DF (2013) A new method for detecting exchanging amide protons using chemical exchange rotation transfer. Magn Reson Med 69:637–647

    Article  CAS  PubMed  Google Scholar 

  35. Lemaire L, Franconi F, Saint-Andre JP, Roullin VG, Jallet P, Le Jeune JJ (2000) High-field quantitative transverse relaxation time, magnetization transfer and apparent water diffusion in experimental rat brain tumour. NMR Biomed 13:116–123

    Article  CAS  PubMed  Google Scholar 

  36. McCreary CR, Bjarnason TA, Skihar V, Mitchell JR, Yong VW, Dunn JF (2009) Multiexponential T2 and magnetization transfer MRI of demyelination and remyelination in murine spinal cord. NeuroImage 45:1173–1182

    Article  PubMed  PubMed Central  Google Scholar 

  37. Mossahebi P, Yarnykh VL, Samsonov A (2014) Analysis and correction of biases in cross-relaxation MRI due to biexponential longitudinal relaxation: modified Cross-Relaxation Imaging (mCRI). Magn Reson Med 71:830–838

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

V.P. received support from IRME and the A*MIDEX grant (n°ANR-11-IDEX-0001-02) funded by the French Government “Investissements d’Avenir” program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guillaume Duhamel.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Human and animal rights

Animal studies were conducted in agreement with the French guidelines for animal care from the French Department of Agriculture (Animal Rights Division), the European Council Directive 86/609/EEC of 24 November 1986, and approved by our institutional committee on ethics in animal research.

Additional information

Valentin H. Prevost and Olivier M. Girard have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prevost, V.H., Girard, O.M., Varma, G. et al. Minimizing the effects of magnetization transfer asymmetry on inhomogeneous magnetization transfer (ihMT) at ultra-high magnetic field (11.75 T). Magn Reson Mater Phy 29, 699–709 (2016). https://doi.org/10.1007/s10334-015-0523-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10334-015-0523-2

Keywords

Navigation