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Physics, Techniques and Review of Neuroradiological Applications of Diffusion Kurtosis Imaging (DKI)

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Abstract

In recent years many papers about diagnostic applications of diffusion tensor imaging (DTI) have been published. This is because DTI allows to evaluate in vivo and in a non-invasive way the process of diffusion of water molecules in biological tissues. However, the simplified description of the diffusion process assumed in DTI does not permit to completely map the complex underlying cellular components and structures, which hinder and restrict the diffusion of water molecules. These limitations can be partially overcome by means of diffusion kurtosis imaging (DKI). The aim of this paper is the description of the theory of DKI, a new topic of growing interest in radiology. DKI is a higher order diffusion model that is a straightforward extension of the DTI model. Here, we analyze the physics underlying this method, we report our MRI acquisition protocol with the preprocessing pipeline used and the DKI parametric maps obtained on a 1.5 T scanner, and we review the most relevant clinical applications of this technique in various neurological diseases.

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References

  1. Colagrande S, Pallotta S, Vanzulli A, Napolitano M, Villari N. The diffusion parameter in magnetic resonance: physics, techniques, and semeiotics. La Radiologia Medica. 2004;109(1–2):1–16.

  2. Colagrande S, Carbone SF, Carusi LM, Cova M, Villari N. Magnetic resonance diffusion–weighted imaging: extraneurological applications. La radiologia medica. 2006;111(3):392–419.

  3. Cappabianca S, Iaselli F, Reginelli A, D'Andrea A, Urraro F, Grassi R, Rotondo A. Value of diffusion-weighted magnetic resonance imaging in the characterization of complex adnexal masses. Tumori. 2013;99(2):210–7.

  4. Mascalchi M, Filippi M, Floris R, Fonda C, Gasparotti R, Villari N. Diffusion-weighted MR of the brain: methodology and clinical application. La Radiologia Medica. 2005;109(3):155–97.

  5. Conti A, Pontoriero A, Ricciardi GK, Granata F, Vinci S, Angileri FF, Pergolizzi S, Alafaci C, Rizzo V, Quartarone A, Germanò A, Foroni RI, De Renzis C, Tomasello F. Integration of functional neuroimaging in cyberknife radiosurgery: feasibility and dosimetric results. Neurosurg Focus. 2013;34(4):E5.

  6. De Nunzio G, Pastore G, Donativi M, Castellano A, Falini A. A CAD system for cerebral glioma based on texture features in DT-MR images. Nucl Instrum Methods Phys Res Sect A. 2011;648:S100–2.

  7. Grinberg F, Farrher E, Ciobanu L, Geffroy F, Bihan DL, Shah NJ. Non-Gaussian Diffusion Imaging for Enhanced Contrast of Brain Tissue Affected by Ischemic Stroke. PloS one. 2014;9(2):e89225.

  8. De Santis S, Gabrielli A, Palombo M, Maraviglia B, Capuani S. Non-Gaussian diffusion imaging: a brief practical review. Magn Reson Imaging. 2011;29(10):1410–6.

  9. Assaf Y, Cohen Y. Non-Mono-Exponential Attenuation of Water and N-Acetyl Aspartate Signals Due to Diffusion in Brain Tissue. J Magn Reson. 1998;131(1):69–85.

  10. Basser PJ, Jones DK. Diffusion-tensor MRI: theory, experimental design and data analysis–a technical review. NMR Biomed. 2002;15(7–8):456–67.

  11. Mariana Lazar JHJ, Xuan L, A Helpern J. Estimation of the orientation distribution function from diffusional kurtosis imaging. Magn Reson Med. 2008;60(4):774–81.

  12. Tuch DS, Reese TG, Wiegell MR, Makris N, Belliveau JW, Van Wedeen J. High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn Reson Med. 2002;48(4):577–82.

  13. 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(6):1432–40.

  14. Wu EX, Cheung MM. MR diffusion kurtosis imaging for neural tissue characterization. NMR Biomed. 2010;23(7):836–48.

  15. Helpern JA, Adisetiyo V, Falangola MF, Hu C, Di Martino A, Williams K, Castellanos FX, Jensen JH. 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(1):17–23.

  16. Veraart J, Poot DHJ, Van Hecke W, Blockx I, Van der Linden A, Verhoye M, Sijbers J. More accurate estimation of diffusion tensor parameters using diffusion kurtosis imaging. Magn Reson Med. 2011;65(1):138–45.

  17. Veraart J, Van Hecke W, Sijbers J. Constrained maximum likelihood estimation of the diffusion kurtosis tensor using a Rician noise model. Magn Reson Med. 2011;66(3):678–86.

  18. Eichner C, Cauley SF, Cohen-Adad J, Möller HE, Turner R. Setsompop K, Wald LL. Real diffusion-weighted MRI enabling true signal averaging and increased diffusion contrast. Neuroimage. 2015;122:373–84.

  19. Assaf Y, Basser PJ. Composite hindered and restricted model of diffusion (charmed) mr imaging of the human brain. Neuroimage. 2005;27(1):48–58.

  20. Alexander DC, Hubbard PL, Hall MG, Moore EA, Ptito M, Parker GJM, Dyrby TB. Orientationally invariant indices of axon diameter and density from diffusion mri. Neuroimage. 2010;52(4):1374–1389.

  21. Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC. Noddi: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage. 2012;61(4):1000–16.

  22. Tabesh A, Jensen JH, Ardekani BA, Helpern JA. Estimation of tensors and tensor-derived measures in diffusional kurtosis imaging. Magn Reson Med. 2011;65(3):823–36.

  23. Kuder TA, Stieltjes B, Bachert P, Semmler W, Laun FB. Advanced fit of the diffusion kurtosis tensor by directional weighting and regularization. Magn Reson Med. 2012;67(5):1401–11.

  24. Reese TG, Heid O, Weisskoff RM, Wedeen VJ. Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn Reson Med. 2003;49(1):177–82.

  25. Pierpaoli C, Walker L, Irfanoglu MO, Barnett A, Basser P, Chang LC, Koay C, Pajevic S, Rohde G, Sarlls J, Wu M. TORTOISE: an integrated software package for processing of diffusion MRI data. Proceedings 18th Scientific Meeting, International Society for Magnetic Resonance in Medicine. 2010.

  26. Collura G, Marrale M, Toschi N, Gagliardo C, Midiri M, Brai M. Sviluppo di un software per l’analisi di immagini di Diffusion Kurtosis Imaging. Proceedings AIRP - Atti del XXXVI Convegno Nazionale di Radioprotezione, Palermo, 18–20 settembre 2013. 2013.

  27. Lätt J, Nilsson M, Wirestam R, St\aahlberg F, Karlsson N, Johansson M, Sundgren PC, van Westen D. Regional values of diffusional kurtosis estimates in the healthy brain. J Magn Reson Imaging. 2013;37(3):610–8.

  28. Beaulieu C. The basis of anisotropic water diffusion in the nervous system–a technical review. NMR Biomed. 2002;15(7–8):435–55.

  29. Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson Series B. 1996;111(3):209–19.

  30. Chincarini A, Bosco P, Gemme G, Morbelli S, Arnaldi D, Sensi F, Solano I, Amoroso N, Tangaro S, Longo R, Squarcia S, Nobili F. Alzheimers disease markers from structural MRI and FDG-PET brain images. Eur Phys J Plus. 2012;127(11):1–16.

  31. Nobili F, Arnaldi D, Roccatagliata L, Chincarini A, Accardo J, Picco A, Ferrara M, Buschiazzo A, Morbelli S. Neuroimaging Findings in Mild Cognitive Impairment. PET and SPECT Neurol. 2014;271–307.

  32. Yablonskiy DA, Bretthorst GL, Ackerman JJH. Statistical model for diffusion attenuated MR signal. Magn Reson Med. 2003;50(4):664–9.

  33. Hui ES, Cheung MM, Qi L, Wu EX. Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis. Neuroimage. 2008;42(1):122–34.

  34. Sevick RJ, Kucharczyk J, Mintorovitch J, Moseley ME, Derugin N, Norman D. Diffusion-weighted MR imaging and T2-weighted MR imaging in acute cerebral ischaemia: comparison and correlation with histopathology. Acta Neurochir Suppl (Wien). 1990;51:210-2.

  35. Hu C, Jensen JH, Falangola MF, Helpern JA. CSF partial volume effect for diffusion kurtosis imaging. Proceedings 16th Scientific Meeting, International Society for Magnetic Resonance in Medicine. 2008.

  36. Hui ES, Fieremans E, Jensen JH, Tabesh A, Feng W, Bonilha L, Spampinato MV, Adams R, Helpern JA. Stroke assessment with diffusional kurtosis imaging. Stroke. 2012;43(11):2968–73.

  37. Falangola MF, Jensen JH, Tabesh A, Hu C, Deardorff RL, Babb JS, Ferris S, A Helpern J. Non-Gaussian diffusion MRI assessment of brain microstructure in mild cognitive impairment and Alzheimers disease. Magn Reson Imaging. 2013;31(6):840–6.

  38. Guo AC, MacFall JR, Provenzale JM. Multiple sclerosis: diffusion tensor mr imaging for evaluation of normal-appearing white matter 1. Radiology. 2002;222(3):729–36.

  39. Rovaris M, Agosta F, Pagani E, Filippi M. Diffusion tensor mr imaging. Neuroimaging Clin N Am. 2009;19(1):37–43.

  40. Werring DJ, Brassat D, Droogan AG, Clark CA, Symms MR, Barker GJ, MacManus DG, Thompson AJ, Miller DH. The pathogenesis of lesions and normal-appearing white matter changes in multiple sclerosis a serial diffusion mri study. Brain. 2000;123(8):1667–76.

  41. Scanderbeg AC, 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 Neuroradiol. 2000;21(5):862–8.

  42. Kamagata K, Tomiyama H, Motoi Y, Kano M, Abe O, Ito K, Shimoji K, Suzuki M, Hori M, Nakanishi A, et al. Diffusional kurtosis imaging of cingulate fibers in Parkinson disease: comparison with conventional diffusion tensor imaging. Magn Reson Imaging. 2013;31(9):1501–6.

  43. Wang J-J, Lin W-Y, Lu C-S, Weng Y-H, Ng S-H, Wang C-H, Liu H-L, Hsieh R-H, Wan Y-L, Wai Y-Y. Parkinson disease: diagnostic utility of diffusion kurtosis imaging. Radiology. 2011;261(1):210–7.

  44. Van Cauter S, Veraart J, Sijbers J, Peeters RR, Himmelreich U, De Keyzer F, Van Gool SW, Van Calenbergh F, De Vleeschouwer S, Van Hecke W, Sunaert S. Gliomas: diffusion kurtosis MR imaging in grading. Radiology. 2012;263(2):492–501.

  45. Gons RAR, de Laat KF, van Norden AGW, van Oudheusden LGB, van Uden IWM, Norris DG, Zwiers MP, de Leeuw FE. Hypertension and cerebral diffusion tensor imaging in small vessel disease. Stroke. 2010;41(12):2801–6.

  46. MacLullich AMJ, Ferguson KJ, Reid LM, Deary IJ, Starr JM, Seckl JR, Bastin ME, Wardlaw JM. Higher systolic blood pressure is associated with increased water diffusivity in normal-appearing white matter. Stroke. 2009;40(12):3869–71.

  47. Shimoji K, Uka T, Tamura Y, Yoshida M, Kamagata K, Hori M, Motoi Y, Watada H, Kawamori R, Aoki S. Diffusional kurtosis imaging analysis in patients with hypertension. Jpn J Radiol. 2014;32(2):98–104.

  48. Zhang Y, Yan X, Gao Y, Xu D, Wu J, Li Y. A preliminary study of epilepsy in children using diffusional kurtosis imaging. Clin Neuroradiol. 2013;23(4):293–300.

  49. Lee C-Y, Tabesh A, Benitez A, Helpern JA, Jensen JH, Bonilha L. Microstructural integrity of early-versus late-myelinating white matter tracts in medial temporal lobe epilepsy. Epilepsia. 2013;54(10):1801–9.

  50. Solarino M, Iovane A, Sutera R. Principi di diagnostica per immagini in medicina dello sport, chapter 18, pages 163–80. EdiSES, 1 edition, 2014. Trauma cranico nello sport. by Gagliardo, C and La Tona, G and Iovane, A.

  51. Grossman EJ, Jensen JH, Babb JS, Chen Q, Tabesh A, Fieremans E, **a D, Inglese M, Grossman RI. Cognitive impairment in mild traumatic brain injury: a longitudinal diffusional kurtosis and perfusion imaging study. AJNR Am J Neuroradiol. 2013;34(5):951–7.

  52. Zhuo J, Xu S, Proctor JL, Mullins RJ, Simon JZ, Fiskum G, Gullapalli RP. Diffusion kurtosis as an in vivo imaging marker for reactive astrogliosis in traumatic brain injury. Neuroimage. 2012;59(1):467–77.

  53. Jensen JH, Helpern JA. MRI quantification of non-Gaussian water diffusion by kurtosis analysis. NMR Biomed. 2010;23(7):698–710.

  54. 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(2):236–47.

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Acknowledgement

The research described in this paper was supported by University of Palermo and by the Project “PON Smart Cities PON04a2_C SMART HEALTH – CLUSTER OSDH – SMART FSE - STAYWELL”, and by the “NextMR” Project (Project Leader: A. Chincarini) funded by the Istituto Nazionale di Fisica Nucleare (INFN).

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Authors and Affiliations

  1. Department of Physics and Chemistry, University of Palermo, Palermo, Italy

    M. Marrale PhD, G. Collura MSc &  M. Brai

  2. Medical Physics Section, Department of Biomedicine and Prevention, University of Rome “Tor Vergata”, Rome, Italy

    N. Toschi PhD

  3. Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Boston, MA, USA

    N. Toschi PhD

  4. Harvard Medical School, Boston, MA, USA

    N. Toschi PhD

  5. University of Palermo, Palermo, Italy

    F. Midiri

  6. Department of Biopathology and Medical Biotechnologies, Section of Radiological Sciences, University of Palermo, Palermo, Italy

    G. La Tona MD, A. Lo Casto MD & C. Gagliardo MD, PhD

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  1. M. Marrale PhD
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Marrale, M., Collura, G., Brai, M. et al. Physics, Techniques and Review of Neuroradiological Applications of Diffusion Kurtosis Imaging (DKI). Clin Neuroradiol 26, 391–403 (2016). https://doi.org/10.1007/s00062-015-0469-9

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