Sources of variation in multi-centre brain MTR histogram studies: body-coil transmission eliminates inter-centre differences

  • P. S. Tofts
  • S. C. A. Steens
  • M. Cercignani
  • F. Admiraal-Behloul
  • P. A. M. Hofman
  • M. J. P. van Osch
  • W. M. Teeuwisse
  • D. J. Tozer
  • J. H. T. M. van Waesberghe
  • R. Yeung
  • G. J. Barker
  • M. A. van Buchem
Research Article

Abstract

Object: 1. Identify sources of variation affecting Magnetisation Transfer Ratio (MTR) histogram reproducibility between-centres. 2. Demonstrate complete elimination of inter-centre difference.

Materials and methods: Six principle sources of variation were summarised and analysed. These are:

the imager coil used for radiofrequency (RF) transmission, imager stability, the shape and other parameters describing the Magnetisation Transfer (MT) pulse, the MT sequence used (including its parameters), the image segmentation methodology, and the histogram generation technique. Transmit field nonuniformity and B1 errors are often the largest factors. PLUMB (Peak Location Uniformity in MTR histograms of the Brain) plots are a convenient way of visualising differences. Five multi-centres studies were undertaken to investigate and minimise differences.

Results: Transmission using a body coil, with a close-fitting array of surface coils for reception, gave the best uniformity. Differences between two centres, having MR imagers from different manufacturers, were completely eliminated by using body coil excitation, making a small adjustment to the MT pulse flip angle, and carrying out segmentation at a single centre. Histograms and their peak location and height values were indistinguishable.

Conclusions: Body coil excitation is preferred for multi-centre studies. Analysis (segmentation and histogram generation) should ideally be carried out at a single site.

Keywords

MRI Brain Magnetisation transfer Multi-centre study 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    van Buchem MA, Tofts PS (2000) Magnetization transfer imaging. Neuroimaging Clin N Am 10:771–788PubMedGoogle Scholar
  2. 2.
    Tofts PS, Steens SCA, van Buchem MA (2003) MT: magnetization transfer (chapter 8). In: Tofts PS (ed.) Quantitative MRI of the brain: measuring changes caused by disease. Wiley, Chichester, pp. 257–298Google Scholar
  3. 3.
    Tofts PS, Davies GR, Dehmeshki J (2003) Histograms: measuring subtle diffuse disease (chapter 18). In: Tofts PS (eds). Quantitative MRI of the brain: measuring changes caused by disease. Wiley, Chichester, pp. 581–610Google Scholar
  4. 4.
    van Buchem MA, Udupa JK, McGowan JC, Miki Y, Heyning FH, Boncoeur-Martel MP, Kolson DL, Polansky M, Grossman RI (1997) Global volumetric estimation of disease burden in multiple sclerosis based on magnetization transfer imaging. AJNR Am J Neuroradiol 18:1287–1290PubMedGoogle Scholar
  5. 5.
    Rovaris M, Bozzali M, Rodegher M, Tortorella C, Comi G, Filippi M (1999) Brain MRI correlates of magnetization transfer imaging metrics in patients with multiple sclerosis. J Neurol Sci 166:58–63PubMedCrossRefGoogle Scholar
  6. 6.
    van Waesberghe JH, van Buchem MA, Filippi M, Castelijns JA, Rocca MA, van der BR, Polman CH, Barkhof F (1998) MR outcome parameters in multiple sclerosis: comparison of surface-based thresholding segmentation and magnetization transfer ratio histographic analysis in relation to disability (a preliminary note). AJNR Am J Neuroradiol 19:1857–1862PubMedGoogle Scholar
  7. 7.
    Filippi M, Iannucci G, Tortorella C, Minicucci L, Horsfield MA, Colombo B, Sormani MP, Comi G (1999) Comparison of MS clinical phenotypes using conventional and magnetization transfer MRI. Neurology 52:588–594PubMedGoogle Scholar
  8. 8.
    Davies GR, Ramio-Torrenta L, Hadjiprocopis A, Chard DT, Griffin CM, Rashid W, Barker GJ, Kapoor R, Thompson AJ, Miller DH (2004) Evidence for grey matter MTR abnormality in minimally disabled patients with early relapsing-remitting multiple sclerosis. J Neurol Neurosurg Psychiatr 75:998–1002PubMedCrossRefGoogle Scholar
  9. 9.
    Bsma GP, Rood MJ, Huizinga TW, de Jong BA, Bollen EL, van Buchem MA (2000) Detection of cerebral involvement in patients with active neuropsychiatric systemic lupus erythematosus by the use of volumetric magnetization transfer imaging. Arthritis Rheum 43:2428–2436PubMedCrossRefGoogle Scholar
  10. 10.
    Steens SC, Admiraal-Behloul F, Bosma GP, Steup-Beekman GM, Olofsen H, Le CS, Huizinga TW, van Buchem MA (2004) Selective gray matter damage in neuropsychiatric lupus. Arthritis Rheum 50:2877–2881PubMedCrossRefGoogle Scholar
  11. 11.
    Patel UJ, Grossman RI, Phillips MD, Udupa JK, McGowan JC, Miki Y, Wei L, Polansky M, van Buchem MA, Kolson D (1999) Serial analysis of magnetization-transfer histograms and Expanded Disability Status Scale scores in patients with relapsing–remitting multiple sclerosis. AJNR Am J Neuroradiol 20:1946–1950PubMedGoogle Scholar
  12. 12.
    Rocca MA, Mastronardo G, Rodegher M, Comi G, Filippi M (1999) Long-term changes of magnetization transfer-derived measures from patients with relapsing–remitting and secondary progressive multiple sclerosis. AJNR Am J Neuroradiol 20:821–827PubMedGoogle Scholar
  13. 13.
    Filippi M, Inglese M, Rovaris M, Sormani MP, Horsfield P, Iannucci PG, Colombo B, Comi G (2000) Magnetization transfer imaging to monitor the evolution of MS: a 1-year follow-up study. Neurology 55:940–946PubMedGoogle Scholar
  14. 14.
    Rovaris M, Agosta F, Sormani MP, Inglese M, Martinelli V, Comi G, Filippi M (2003) Conventional and magnetization transfer MRI predictors of clinical multiple sclerosis evolution: a medium-term follow-up study. Brain 126:2323–2332PubMedCrossRefGoogle Scholar
  15. 15.
    Davies GR, Altmann DR, Rashid W, Chard DT, Griffin CM, Barker GJ, Kapoor R, Thompson AJ, Miller DH (2005) Emergence of thalamic magnetization transfer ratio abnormality in early relapsing–remitting multiple sclerosis. Mult Scler 11:276–281PubMedCrossRefGoogle Scholar
  16. 16.
    Davies GR, Altmann DR, Hadjiprocopis A, Rashid W, Chard DT, Griffin CM, Tofts PS, Barker GJ, Kapoor R, Thompson AJ, Miller DH (2005) Increasing normal-appearing grey and white matter magnetisation transfer ratio abnormality in early relapsing–remitting multiple sclerosis. J Neurol 252:1037–1044PubMedCrossRefGoogle Scholar
  17. 17.
    Berry I, Barker GJ, Barkhof F, Campi A, Dousset V, Franconi JM, Gass A, Schreiber W, Miller DH, Tofts PS (1999) A multicenter measurement of magnetization transfer ratio in normal white matter. J Magn Reson Imaging 9:441–446PubMedCrossRefGoogle Scholar
  18. 18.
    Barker GJ, Tofts PS, Gass A (1996) An interleaved sequence for accurate and reproducible clinical measurement of magnetization transfer ratio. Magn Reson Imaging 14:403–411PubMedCrossRefGoogle Scholar
  19. 19.
    Sormani MP, Iannucci G, Rocca MA, Mastronardo G, Cercignani M, Minicucci L, Filippi M (2000) Reproducibility of magnetization transfer ratio histogram-derived measures of the brain in healthy volunteers. AJNR Am J Neuroradiol 21:133–136PubMedGoogle Scholar
  20. 20.
    Horsfield MA, Barker GJ, Barkhof F, Miller DH, Thompson AJ, Filippi M (2003) Guidelines for using quantitative magnetization transfer magnetic resonance imaging for monitoring treatment of multiple sclerosis. J Magn Reson Imaging 17:389–397PubMedCrossRefGoogle Scholar
  21. 21.
    Tofts PS, Steens SCA, Dehmeshki J, Hofman P, van Waesberghe JH, van Buchem MA (2001) Matching MTR histograms for Multi-Centre Studies. In: Proceedings of the International Society for magnetic resonance in medicine, 9th annual meeting, Glasgow, pp. 1380Google Scholar
  22. 22.
    Tofts PS, Yeung R, Barker GJ (2002) Improvement in MTR histogram multi-centre performance using a receive-only head coil: the PLUMB plot. In: Proceedings of the International Society for magnetic resonance in medicine, 10th annual meeting, Honolulu, pp. 2283Google Scholar
  23. 23.
    Tofts PS, Steens SC, Cercignani M, Tozer DJ, Teeuwisse WM, van Osch MJ, Admiraal-Behloul F, Barker GJ, van Buchem MA (2006) Intercentre differences in multicentre brain MTR histogram studies can almost be eliminated by using body coil transmission. In: Proceedings of the International Society for magnetic resonance in medicine, 14th annual meeting, SeattleGoogle Scholar
  24. 24.
    Ropele S, Filippi M, Valsasina P, Korteweg T, Barkhof F, Tofts PS, Samson R, Miller DH, Fazekas F (2004) Assessment and correction of B(1)-induced errors in magnetization transfer ratio measurements. Magn Reson Med 53:134–140CrossRefGoogle Scholar
  25. 25.
    Samson RS, Wheeler-Kingshott CA, Symms MR, Tozer DJ, Tofts PS (2006) A simple correction for B1 field errors in magnetization transfer ratio measurements. Magn Reson Imaging 24(3):255–263PubMedCrossRefGoogle Scholar
  26. 26.
    Barker GJ, Schreiber WG, Gass A, Ranjeva JP, Campi A, van Waesberghe JH, Franconi JM, Watt HC, Tofts PS (2005) A standardised method for measuring magnetisation transfer ratio on MR imagers from different manufacturers – the EuroMT sequence. Magn Reson Mater Phy 18:76–80CrossRefGoogle Scholar
  27. 27.
    Pekar J, Jezzard P, Roberts DA, Leigh Jr JS, Frank JA, McLaughlin AC (1996) Perfusion imaging with compensation for asymmetric magnetization transfer effects. Magn Reson Med 35:70–79PubMedCrossRefGoogle Scholar
  28. 28.
    van Buchem MA, McGowan JC, Kolson DL, Polansky M, Grossman RI (1996) Quantitative volumetric magnetization transfer analysis in multiple sclerosis: estimation of macroscopic and microscopic disease burden. Magn Reson Med 36:632–636PubMedCrossRefGoogle Scholar
  29. 29.
    Cercignani M, Symms MR, Schmierer K, Boulby PA, Tozer DJ, Ron M, Tofts PS, Barker GJ (2005) Three-dimensional quantitative magnetisation transfer imaging of the human brain. Neuroimage 27:436–441PubMedCrossRefGoogle Scholar
  30. 30.
    Stevenson VL, Parker GJ, Barker GJ, Birnie K, Tofts PS, Miller DH, Thompson AJ (2000) Variations in T1 and T2 relaxation times of normal appearing white matter and lesions in multiple sclerosis. J Neurol Sci 178:81–87PubMedCrossRefGoogle Scholar
  31. 31.
    Tofts PS (2003) PD: proton density of tissue water (chapter 4). In: Tofts PS (ed) Quantitative MRI of the brain: measuring change caused by disease. Wiley, Chichester, pp. 85–109Google Scholar
  32. 32.
    Jost G, Hahnel S, Heiland S, Stippich C, Bellemann ME, Sartor K (2002) An automated method for volumetric quantification of magnetization transfer of the brain. Magn Reson Imaging 20:593–597PubMedCrossRefGoogle Scholar
  33. 33.
    Tozer DJ, Tofts PS (2003) Removing spikes caused by quantization noise from high-resolution histograms. Magn Reson Med 50:649–653PubMedCrossRefGoogle Scholar
  34. 34.
    Fernando KT, Tozer DJ, Miszkiel KA, Gordon RM, Swanton JK, Dalton CM, Barker GJ, Plant GT, Thompson AJ, Miller DH (2005) Magnetization transfer histograms in clinically isolated syndromes suggestive of multiple sclerosis. Brain 128:2911–2925PubMedCrossRefGoogle Scholar
  35. 35.
    Hofman PA, Kemerink GJ, Jolles J, Wilmink JT (1999) Quantitative analysis of magnetization transfer images of the brain: effect of closed head injury, age and sex on white matter. Magn Reson Med 42:803–806PubMedCrossRefGoogle Scholar
  36. 36.
    Dehmeshki J, Barker GJ, Tofts PS (2002) Classification of disease subgroup and correlation with disease severity using magnetic resonance imaging whole-brain histograms: application to magnetization transfer ratios and multiple sclerosis. IEEE Trans Med Imaging 21:320–331PubMedCrossRefGoogle Scholar
  37. 37.
    Udupa JK, Odhner D, Samarasekera S, Goncalves RJ, Venugopal KP, Furule SS (1994) 3DVIEWUNIX: an open, transportable, multidimensional, multimodality, multiparametric imaging software system. SPIE Proc 2164:58–73CrossRefGoogle Scholar
  38. 38.
    Silver NC, Barker GJ, Gass A, Schreiber W, Miller DH, Tofts PS (1997) Magnetisation transfer ratio measurements of the brain depend on the region of interest position within the head coil. In: Proceedings of the International Society of magnetic resonance in medicine, 5th Annual meeting, Vancouver, pp. 662Google Scholar
  39. 39.
    Barker GJ, Simmons A, Arridge SR, Tofts PS (1998) A simple method for investigating the effects of non-uniformity of radiofrequency transmission and radiofrequency reception in MRI. Br J Radiol 71:59–67PubMedGoogle Scholar
  40. 40.
    Whittall KP, MacKay AL, Graeb DA, Nugent RA, Li DK, Paty DW (1997) In vivo measurement of T2 distributions and water contents in normal human brain. Magn Reson Med 37:34–43PubMedCrossRefGoogle Scholar
  41. 41.
    Graham SJ, Henkelman RM (1999) Pulsed magnetization transfer imaging: evaluation of technique. Radiology 212:903–910PubMedGoogle Scholar
  42. 42.
    Tofts PS (1994) Standing waves in uniform water phantoms. J Magn Reson series B 104:143–147CrossRefGoogle Scholar
  43. 43.
    Collins CM, Smith MB (2001) Signal-to-noise ratio and absorbed power as functions of main magnetic field strength, and definition of “90 degrees ” RF pulse for the head in the birdcage coil. Magn Reson Med 45:684–691PubMedCrossRefGoogle Scholar
  44. 44.
    Tofts PS, Benton CE, Tozer DJ, Jäger HR, Waldman AD, Rees JH (2005) Quantitative histogram analysis of Gd enhancement in low grade gliomas may predict malignant transformation. In: Proceedings of the International Society for magnetic resonance in medicine, 13th annual meeting, Miami, p. 754Google Scholar
  45. 45.
    Scheid F (1968) Schaum’s outline of theory and problems of numerical analysis. McGraw–Hill, New YorkGoogle Scholar
  46. 46.
    Ramani A, Dalton C, Miller DH, Tofts PS, Barker GJ (2002) Precise estimate of fundamental in-vivo MT parameters in human brain in clinically feasible times. Magn Reson Imaging 20:721–731PubMedCrossRefGoogle Scholar
  47. 47.
    Sled JG, Pike GB (2001) Quantitative imaging of magnetization transfer exchange and relaxation properties in vivo using MRI. Magn Reson Med 46:923–931PubMedCrossRefGoogle Scholar
  48. 48.
    Yarnykh VL (2002) Pulsed Z-spectroscopic imaging of cross-relaxation parameters in tissues for human MRI: theory and clinical applications. Magn Reson Med 47:929–939PubMedCrossRefGoogle Scholar
  49. 49.
    Tofts PS, Cercignani M, Tozer DJ, Symms MR, Davies GR, Ramani A, Barker GJ (2005) Errata: Tozer et al. Quantitative magnetization transfer mapping of bound protons in multiple sclerosis, Magn Reson Med 2003;50:83–91. Magn Reson Med 53:492–493Google Scholar

Copyright information

© ESMRMB 2006

Authors and Affiliations

  • P. S. Tofts
    • 1
    • 6
  • S. C. A. Steens
    • 2
  • M. Cercignani
    • 1
  • F. Admiraal-Behloul
    • 2
  • P. A. M. Hofman
    • 3
  • M. J. P. van Osch
    • 2
  • W. M. Teeuwisse
    • 2
  • D. J. Tozer
    • 1
  • J. H. T. M. van Waesberghe
    • 4
  • R. Yeung
    • 5
  • G. J. Barker
    • 1
    • 7
  • M. A. van Buchem
    • 2
  1. 1.Institute of NeurologyUniversity College LondonLondonUK
  2. 2.Department of RadiologyLeiden University Medical CenterLeidenNetherlands
  3. 3.Department of RadiologyMaastricht University HospitalMaastrichtNetherlands
  4. 4.Department of RadiologyFree University Medical CentreAmsterdamNetherlands
  5. 5.GE Medical SystemsSloughUK
  6. 6.Brighton and Sussex Medical SchoolBrightonUK
  7. 7.King’s College London, Institute of Psychiatry (Box 089), Department of Clinical NeuroscienceCentre for Neuroimaging SciencesLondonUK

Personalised recommendations