Does diffusion kurtosis imaging lead to better neural tissue characterization? A rodent brain maturation study

Diffusion kurtosis imaging (DKI) can be used to estimate excess kurtosis, which is a dimensionless measure for the deviation of water diffusion profile from Gaussian distribution. Several recent studies have applied DKI to probe the restricted water diffusion in biological tissues. The directional analysis has also been developed to obtain the directionally specific kurtosis. However, these studies could not directly evaluate the sensitivity of DKI in detecting subtle neural tissue alterations. Brain maturation is known to involve various biological events that can affect water diffusion properties, thus providing a sensitive platform to evaluate the efficacy of DKI. In this study, in vivo DKI experiments were performed in normal Sprague-Dawley rats of 3 different ages: postnatal days 13, 31 and 120 (N=6 for each group). Regional analysis was then performed for 4 white matter (WM) and 3 gray matter (GM) structures. Diffusivity and kurtosis estimates derived from DKI were shown to be highly sensitive to the developmental changes in these chosen structures. Conventional diffusion tensor imaging (DTI) parameters were also computed using monoexponential model, yielding reduced sensitivity and directional specificity in monitoring the brain maturation changes. These results demonstrated that, by measuring directionally specific diffusivity and kurtosis, DKI offers a more comprehensive and sensitive detection of tissue microstructural changes. Such imaging advance can provide a better MR diffusion characterization of neural tissues, both WM and GM, in normal, developmental and pathological states.

[1]  Stephan E Maier,et al.  Developmental changes and injury induced disruption of the radial organization of the cortex in the immature rat brain revealed by in vivo diffusion tensor MRI. , 2007, Cerebral cortex.

[2]  Yoram Cohen,et al.  Spatial and temporal damage evolution after hemi-crush injury in rat spinal cord obtained by high b-value q-space diffusion magnetic resonance imaging. , 2007, Journal of neurotrauma.

[3]  J. Helpern,et al.  Three‐dimensional characterization of non‐gaussian water diffusion in humans using diffusion kurtosis imaging , 2006, NMR in biomedicine.

[4]  Y. Cohen,et al.  Non-mono-exponential attenuation of water and N-acetyl aspartate signals due to diffusion in brain tissue. , 1998, Journal of magnetic resonance.

[5]  D. Le Bihan,et al.  Water diffusion compartmentation and anisotropy at high b values in the human brain , 2000, Magnetic resonance in medicine.

[6]  Ludovico Minati,et al.  Biexponential and diffusional kurtosis imaging, and generalised diffusion-tensor imaging (GDTI) with rank-4 tensors: a study in a group of healthy subjects , 2007, Magnetic Resonance Materials in Physics, Biology and Medicine.

[7]  M. Solaiyappan,et al.  Diffusion tensor imaging of the developing mouse brain , 2001, Magnetic resonance in medicine.

[8]  Shu-Wei Sun,et al.  Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia , 2003, NeuroImage.

[9]  J. Tsuruda,et al.  Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. , 1990, Radiology.

[10]  T. Mareci,et al.  Generalized diffusion tensor imaging and analytical relationships between diffusion tensor imaging and high angular resolution diffusion imaging , 2003, Magnetic resonance in medicine.

[11]  Markus Nilsson,et al.  In vivo visualization of displacement-distribution-derived parameters in q-space imaging. , 2008, Magnetic resonance imaging.

[12]  Liqun Qi,et al.  D-eigenvalues of diffusion kurtosis tensors , 2008 .

[13]  Tao Jin,et al.  Functional changes of apparent diffusion coefficient during visual stimulation investigated by diffusion-weighted gradient-echo fMRI , 2008, NeuroImage.

[14]  J. Dubois,et al.  Diffusion tensor imaging of brain development. , 2006, Seminars in fetal & neonatal medicine.

[15]  P A Narayana,et al.  Early postnatal development of rat brain: In vivo diffusion tensor imaging , 2008, Journal of neuroscience research.

[16]  J. A. Helpern,et al.  Assessment of abnormalities in the cerebral microstructure of schizophrenia patients : a diffusional kurtosis imaging study , 2007 .

[17]  Derek K. Jones,et al.  Diffusion‐tensor MRI: theory, experimental design and data analysis – a technical review , 2002 .

[18]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[19]  M. Hedehus,et al.  In vivo mapping of the fast and slow diffusion tensors in human brain , 2002, Magnetic resonance in medicine.

[20]  P. Basser Inferring microstructural features and the physiological state of tissues from diffusion‐weighted images , 1995, NMR in biomedicine.

[21]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[22]  Shu-Leong Ho,et al.  Manganese‐enhanced MRI detection of neurodegeneration in neonatal hypoxic‐ischemic cerebral injury , 2008, Magnetic resonance in medicine.

[23]  Ed X. Wu,et al.  Towards better MR characterization of neural tissues using directional diffusion kurtosis analysis , 2008, NeuroImage.

[24]  N. Makris,et al.  High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity , 2002, Magnetic resonance in medicine.

[25]  D. Norris,et al.  Biexponential diffusion attenuation in various states of brain tissue: Implications for diffusion‐weighted imaging , 1996, Magnetic resonance in medicine.

[26]  R E Snyder,et al.  Changes in water diffusion due to Wallerian degeneration in peripheral nerve , 1996, Magnetic resonance in medicine.

[27]  M. Moseley,et al.  Magnetic Resonance in Medicine 51:924–937 (2004) Characterizing Non-Gaussian Diffusion by Using Generalized Diffusion Tensors , 2022 .

[28]  Hao Huang,et al.  White and gray matter development in human fetal, newborn and pediatric brains , 2006, NeuroImage.

[29]  Jian Yang,et al.  Detection of cortical gray matter lesion in the late phase of mild hypoxic–ischemic injury by manganese-enhanced MRI , 2008, NeuroImage.

[30]  Christos Davatzikos,et al.  Spatiotemporal maturation patterns of murine brain quantified by diffusion tensor MRI and deformation-based morphometry , 2005, Proc. Natl. Acad. Sci. USA.

[31]  Shu-Wei Sun,et al.  Differential sensitivity of in vivo and ex vivo diffusion tensor imaging to evolving optic nerve injury in mice with retinal ischemia , 2006, NeuroImage.

[32]  M. Horsfield,et al.  Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[33]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

[34]  P. Hüppi,et al.  Diffusion tensor imaging of normal and injured developing human brain ‐ a technical review , 2002, NMR in biomedicine.

[35]  H. Pfeifer Principles of Nuclear Magnetic Resonance Microscopy , 1992 .

[36]  T. L. James,et al.  CHAPTER 2 – PRINCIPLES OF NUCLEAR MAGNETIC RESONANCE , 1975 .

[37]  Yoram Cohen,et al.  High b-value q-space diffusion MRI in myelin-deficient rat spinal cords. , 2006, Magnetic resonance imaging.

[38]  Y Wang,et al.  Hypoxic-ischemic brain injury in the neonatal rat model: relationship between lesion size at early MR imaging and irreversible infarction. , 2006, AJNR. American journal of neuroradiology.

[39]  Fahmeed Hyder,et al.  Neurodevelopment of C57B/L6 mouse brain assessed by in vivo diffusion tensor imaging , 2007, NMR in biomedicine.

[40]  Silun Wang,et al.  Characterization of White Matter Injury in a Hypoxic-Ischemic Neonatal Rat Model by Diffusion Tensor MRI , 2008, Stroke.

[41]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[42]  P. Poulet,et al.  Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging , 2006, Journal of neuroscience research.

[43]  Jean-Marie Bonny,et al.  In vivo analysis of the post‐natal development of normal mouse brain by DTI , 2007, NMR in biomedicine.

[44]  Ed X. Wu,et al.  Comparison of directional diffusion kurtoses and diffusivities in EAE-induced spinal cord , 2008 .

[45]  Lucie Hertz-Pannier,et al.  Assessment of the early organization and maturation of infants' cerebral white matter fiber bundles: A feasibility study using quantitative diffusion tensor imaging and tractography , 2006, NeuroImage.

[46]  Talma Hendler,et al.  White matter changes in multiple sclerosis: correlation of q-space diffusion MRI and 1H MRS. , 2005, Magnetic resonance imaging.

[47]  Hsiao-Fang Liang,et al.  Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain , 2005, Magnetic resonance in medicine.

[48]  Hao Huang,et al.  Three-dimensional anatomical characterization of the developing mouse brain by diffusion tensor microimaging , 2003, NeuroImage.

[49]  J. Helpern,et al.  Diffusional kurtosis imaging: The quantification of non‐gaussian water diffusion by means of magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[50]  Yaniv Assaf,et al.  Hypertension and neuronal degeneration in excised rat spinal cord studied by high-b value q-space diffusion magnetic resonance imaging , 2003, Experimental Neurology.

[51]  Joseph A. Helpern,et al.  Quantifying Non-Gaussian Water Diffusion by Means of Pulsed-Field-Gradient MRI , 2003 .

[52]  T. Nakada,et al.  Absolute eigenvalue diffusion tensor analysis for human brain maturation , 2003, NMR in biomedicine.

[53]  C. Westin,et al.  Multi‐component apparent diffusion coefficients in human brain † , 1999, NMR in biomedicine.