Skip to main content

Advertisement

SpringerLink
Log in

Diffusional kurtosis imaging of normal-appearing white matter in multiple sclerosis: preliminary clinical experience

  • Original article
  • Published:
Japanese Journal of Radiology Aims and scope Submit manuscript

Abstract

Purpose

We evaluated diffusional changes in normal-appearing white matter (NAWM) regions remote from multiple sclerosis (MS) plaques by using diffusional kurtosis imaging (DKI) to investigate the non-Gaussian behavior of water diffusion.

Materials and methods

Participants were 11 MS patients and 6 age-matched healthy volunteers. DKI was performed on a 3-T MR imager. Fractional anisotropy (FA), apparent diffusion coefficient (ADC), and diffusional kurtosis (DK) maps were computed. Regions of interest (ROIs) were compared in 24 cerebral regions, including the frontal, parietal, and temporal lobe white matter (WM) in controls and NAWM in MS patients.

Results

The mean FA of all ROIs was 0.468 ± 0.014 (SD) (controls) or 0.431 ± 0.029 (MS group) (P = 0.016). Mean ADC was 0.785 ± 0.034 × 10−3 mm2/s (controls) or 0.805 ± 0.041 × 10−3 mm2/s (MS group). The mean DK of all ROIs was 0.878 ± 0.020 (controls) or 0.823 ± 0.032 (MS group) (P = 0.002). Analysis of individual ROIs revealed significant differences in DK in 3 ROIs between normal WM and NAWM, but significant differences in ADC and FA in only one ROI each.

Conclusion

DKI may be a new sensitive indicator for detecting tissue damage in MS patients in addition to conventional diffusional evaluations, for example diffusion tensor imaging.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging. 2001;13:534–46.

    Article  PubMed  Google Scholar 

  2. Rocca MA, Cercignani M, Iannucci G, Comi G, Filippi M. Weekly diffusion-weighted imaging of normal-appearing white matter in MS. Neurology. 2000;55:882–4.

    Article  PubMed  CAS  Google Scholar 

  3. Cercignani M, Iannucci G, Filippi M. Diffusion-weighted imaging in multiple sclerosis. Ital J Neurol Sci. 1999;20:S246–9.

    Article  PubMed  CAS  Google Scholar 

  4. Horsfield MA, Lai M, Webb SL, Barker GJ, Tofts PS, Turner R, et al. Apparent diffusion coefficients in benign and secondary progressive multiple sclerosis by nuclear magnetic resonance. Magn Reson Med. 1996;36:393–400.

    Article  PubMed  CAS  Google Scholar 

  5. Basser PJ. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 1995;8:333–44.

    Article  PubMed  CAS  Google Scholar 

  6. Guo AC, MacFall JR, Provenzale JM. Multiple sclerosis: diffusion tensor MR imaging for evaluation of normal-appearing white matter. Radiology. 2002;222:729–36.

    Article  PubMed  Google Scholar 

  7. Filippi M, Agosta F. Imaging biomarkers in multiple sclerosis. J Magn Reson Imaging. 2010;31:770–88.

    Article  PubMed  CAS  Google Scholar 

  8. Rovaris M, Agosta F, Pagani E, Filippi M. Diffusion tensor MR imaging. Neuroimaging Clin N Am. 2009;19:37–43.

    Article  PubMed  Google Scholar 

  9. Werring DJ, Brassat D, Droogan AG, Clark CA, Symms MR, Barker GJ, et al. The pathogenesis of lesions and normal-appearing white matter changes in multiple sclerosis: a serial diffusion MRI study. Brain. 2000;123(Pt 8):1667–76.

    Article  PubMed  Google Scholar 

  10. Castriota Scanderbeg A, Tomaiuolo F, Sabatini U, Nocentini U, Grasso MG, Caltagirone C. Demyelinating plaques in relapsing-remitting and secondary-progressive multiple sclerosis: assessment with diffusion MR imaging. AJNR Am J Neuroradiol. 2000;21:862–8.

    PubMed  CAS  Google Scholar 

  11. Tsuchiya K, Hachiya J, Maehara T. Diffusion-weighted MR imaging in multiple sclerosis: comparison with contrast-enhanced study. Eur J Radiol. 1999;31:165–9.

    Article  PubMed  CAS  Google Scholar 

  12. Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med. 2005;53:1432–40.

    Article  PubMed  Google Scholar 

  13. Lu H, Jensen JH, Ramani A, Helpern JA. Three-dimensional characterization of non-gaussian water diffusion in humans using diffusion kurtosis imaging. NMR Biomed. 2006;19:236–47.

    Article  PubMed  Google Scholar 

  14. Hori M, Fukunaga I, Masutani Y, Taoka T, Kamagata K, Suzuki Y, et al. Visualizing non-Gaussian diffusion: clinical application of q-space imaging and diffusional kurtosis imaging of the brain and spine. Magn Reson Med Sci. 2012;11(4):221–8.

    Google Scholar 

  15. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol. 2001;50:121–7.

    Article  PubMed  CAS  Google Scholar 

  16. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69:292–302.

    Article  PubMed  Google Scholar 

  17. Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria”. Ann Neurol. 2005;58:840–6.

    Article  PubMed  Google Scholar 

  18. Kurtzke JF. A new scale for evaluating disability in multiple sclerosis. Neurology. 1955;5:580–3.

    Article  PubMed  CAS  Google Scholar 

  19. Jensen JH, Helpern JA. MRI quantification of non-Gaussian water diffusion by kurtosis analysis. NMR Biomed. 2010;23:698–710.

    Article  PubMed  Google Scholar 

  20. Stejeskal EO, Tanner JE. Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phys. 1965;42:288–92.

    Article  Google Scholar 

  21. McFarlin DE, McFarland HF. Multiple sclerosis (first of two parts). N Engl J Med. 1982;307:1183–8.

    Article  PubMed  CAS  Google Scholar 

  22. McFarlin DE, McFarland HF. Multiple sclerosis (second of two parts). N Engl J Med. 1982;307:1246–51.

    Article  PubMed  CAS  Google Scholar 

  23. Rodriguez M, Siva A, Ward J, Stolp-Smith K, O’Brien P, Kurland L. Impairment, disability, and handicap in multiple sclerosis: a population-based study in Olmsted County Minnesota. Neurology. 1994;44:28–33.

    Article  PubMed  CAS  Google Scholar 

  24. Vigeveno RM, Wiebenga OT, Wattjes MP, Geurts JJ, Barkhof F. Shifting imaging targets in multiple sclerosis: from inflammation to neurodegeneration. J Magn Reson Imaging. 2012;36:1–19.

    Article  PubMed  Google Scholar 

  25. Geurts JJ, Stys PK, Minagar A, Amor S, Zivadinov R. Gray matter pathology in (chronic) MS: modern views on an early observation. J Neurol Sci. 2009;282:12–20.

    Article  PubMed  Google Scholar 

  26. Fazekas F, Barkhof F, Filippi M, Grossman RI, Li DK, McDonald WI, et al. The contribution of magnetic resonance imaging to the diagnosis of multiple sclerosis. Neurology. 1999;53:448–56.

    Article  PubMed  CAS  Google Scholar 

  27. Barkhof F, van Walderveen M. Characterization of tissue damage in multiple sclerosis by nuclear magnetic resonance. Philos Trans R Soc Lond B Biol Sci. 1999;354:1675–86.

    Article  PubMed  CAS  Google Scholar 

  28. Miki Y, Grossman RI, Udupa JK, van Buchem MA, Wei L, Phillips MD, et al. Differences between relapsing-remitting and chronic progressive multiple sclerosis as determined with quantitative MR imaging. Radiology. 1999;210:769–74.

    PubMed  CAS  Google Scholar 

  29. Miki Y, Grossman RI, Udupa JK, Wei L, Polansky M, Mannon LJ, et al. Relapsing-remitting multiple sclerosis: longitudinal analysis of MR images—lack of correlation between changes in T2 lesion volume and clinical findings. Radiology. 1999;213:395–9.

    PubMed  CAS  Google Scholar 

  30. Phillips MD, Grossman RI, Miki Y, Wei L, Kolson DL, van Buchem MA, et al. Comparison of T2 lesion volume and magnetization transfer ratio histogram analysis and of atrophy and measures of lesion burden in patients with multiple sclerosis. AJNR Am J Neuroradiol. 1998;19:1055–60.

    PubMed  CAS  Google Scholar 

  31. Werring DJ, Clark CA, Barker GJ, Thompson AJ, Miller DH. Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis. Neurology. 1999;52:1626–32.

    Article  PubMed  CAS  Google Scholar 

  32. Bammer R, Augustin M, Strasser-Fuchs S, Seifert T, Kapeller P, Stollberger R, et al. Magnetic resonance diffusion tensor imaging for characterizing diffuse and focal white matter abnormalities in multiple sclerosis. Magn Reson Med. 2000;44:583–91.

    Article  PubMed  CAS  Google Scholar 

  33. Abdallah CG, Tang CY, Mathew SJ, Martinez J, Hof PR, Perera TD, et al. Diffusion tensor imaging in studying white matter complexity: a gap junction hypothesis. Neurosci Lett. 2010;475:161–4.

    Article  PubMed  CAS  Google Scholar 

  34. Lazar M, Jensen JH, Xuan L, Helpern JA. Estimation of the orientation distribution function from diffusional kurtosis imaging. Magn Reson Med. 2008;60:774–81.

    Article  PubMed  Google Scholar 

  35. Iraji A, Davoodi-Bojd E, Soltanian-Zadeh H, Hossein-Zadeh GA, Jiang Q. Diffusion kurtosis imaging discriminates patients with white matter lesions from healthy subjects. In: Proceedings of the 33rd international conference of the IEEE engineering in medicine and biology society. 2011. p. 2796–9.

  36. Falangola MF, Jensen JH, Babb JS, Hu C, Castellanos FX, Di Martino A, et al. Age-related non-Gaussian diffusion patterns in the prefrontal brain. J Magn Reson Imaging. 2008;28:1345–50.

    Article  PubMed  Google Scholar 

  37. Cheung MM, Hui ES, Chan KC, Helpern JA, Qi L, Wu EX. Does diffusion kurtosis imaging lead to better neural tissue characterization? A rodent brain maturation study. Neuroimage. 2009;45:386–92.

    Article  PubMed  Google Scholar 

  38. Raab P, Hattingen E, Franz K, Zanella FE, Lanfermann H. Cerebral gliomas: diffusional kurtosis imaging analysis of microstructural differences. Radiology. 2010;254:876–81.

    Article  PubMed  Google Scholar 

  39. Grossman EJ, Ge Y, Jensen JH, Babb JS, Miles L, Reaume J, et al. Thalamus and cognitive impairment in mild traumatic brain injury: a diffusional kurtosis imaging study. J Neurotrauma. 2012;29:2318–27.

    Google Scholar 

  40. Zhuo J, Xu S, Proctor JL, Mullins RJ, Simon JZ, Fiskum G, et al. Diffusion kurtosis as an in vivo imaging marker for reactive astrogliosis in traumatic brain injury. Neuroimage. 2012;59:467–77.

    Article  PubMed  Google Scholar 

  41. Helpern JA, Adisetiyo V, Falangola MF, Hu C, Di Martino A, Williams K, et al. Preliminary evidence of altered gray and white matter microstructural development in the frontal lobe of adolescents with attention-deficit hyperactivity disorder: a diffusional kurtosis imaging study. J Magn Reson Imaging. 2011;33:17–23.

    Article  PubMed  Google Scholar 

  42. Hori M, Aoki S, Fukunaga I, Suzuki Y, Masutani Y. A new diffusion metric, diffusion kurtosis imaging, used in the serial examination of a patient with stroke. Acta Radiol Sh Rep. 2012;1:2.

    Google Scholar 

  43. Trampel R, Jensen JH, Lee RF, Kamenetskiy I, McGuinness G, Johnson G. Diffusional kurtosis imaging in the lung using hyperpolarized 3He. Magn Reson Med. 2006;56:733–7.

    Article  PubMed  Google Scholar 

  44. Allen IV, McQuaid S, Mirakhur M, Nevin G. Pathological abnormalities in the normal-appearing white matter in multiple sclerosis. Neurol Sci. 2001;22:141–4.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was partly supported by a Grant-in-Aid for Scientific Research on Innovative Areas (Comprehensive Brain Science Network) from the Ministry of Education, Science, Sports and Culture of Japan.

Author information

Authors and Affiliations

  1. Department of Radiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo, 113-8431, Japan

    Mariko Yoshida, Masaaki Hori, Michimasa Suzuki, Koji Kamagata, Keigo Shimoji, Atsushi Nakanishi & Shigeki Aoki

  2. Department of Neurology, Juntendo University School of Medicine, Tokyo, Japan

    Kazumasa Yokoyama & Nobutaka Hattori

  3. Graduate School of Health Promotion Science, Tokyo Metropolitan University, Tokyo, Japan

    Issa Fukunaga

  4. Division of Radiology and Biomedical Engineering, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan

    Yoshitaka Masutani

Authors
  1. Mariko Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masaaki Hori
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazumasa Yokoyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Issa Fukunaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michimasa Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Koji Kamagata
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Keigo Shimoji
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Atsushi Nakanishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nobutaka Hattori
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yoshitaka Masutani
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Shigeki Aoki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mariko Yoshida.

About this article

Cite this article

Yoshida, M., Hori, M., Yokoyama, K. et al. Diffusional kurtosis imaging of normal-appearing white matter in multiple sclerosis: preliminary clinical experience. Jpn J Radiol 31, 50–55 (2013). https://doi.org/10.1007/s11604-012-0147-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11604-012-0147-7

Keywords

Search

Navigation