Studies of anomalous diffusion in the human brain using fractional order calculus
It is well known that diffusion‐induced MR signal loss deviates from monoexponential decay, particularly at high b‐values (e.g., >1500 sec/mm2 for human brain tissues). A number of models have been developed to describe this anomalous diffusion behavior and relate the diffusion measurements to ti...
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Published in | Magnetic resonance in medicine Vol. 63; no. 3; pp. 562 - 569 |
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Abstract | It is well known that diffusion‐induced MR signal loss deviates from monoexponential decay, particularly at high b‐values (e.g., >1500 sec/mm2 for human brain tissues). A number of models have been developed to describe this anomalous diffusion behavior and relate the diffusion measurements to tissue structures. Recently, a new diffusion model was proposed by solving the Bloch‐Torrey equation using fractional order calculus with respect to time and space (Magin et al., J Magn Reson 2008;190:255‐270; Zhou et al., Proc Int'l Soc Magn Reson Med 2008). Using a spatial Laplacian ∇2β, this model yields a new set of parameters to describe anomalous diffusion: diffusion coefficient D, fractional order derivative in space β, and a spatial parameter μ (in units of μm). In this study, we demonstrate that the fractional calculus model can be successfully applied to analyzing diffusion images of healthy human brain tissues in vivo. Five human volunteers were scanned on a commercial 3‐T scanner using a customized single‐shot echo‐planar imaging diffusion sequence with 15 b values ranging from 0 to 4700 sec/mm2. The set of images was analyzed using the fractional calculus model, producing spatially resolved maps of D, β, and μ. The β and μ maps showed notable contrast between white and gray matter. The contrast has been attributed to the varying degree of complexity of the underlying tissue structures and microenvironment. Although the biophysical basis of β and μ remains elusive, the potential utility of these parameters to characterize the environment for molecular diffusion, as a complement to apparent diffusion coefficient, may lead to a new way to investigate tissue structural changes in disease progression, intervention, and regression. Magn Reson Med 63:562–569, 2010. © 2010 Wiley‐Liss, Inc. |
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AbstractList | It is well known that diffusion‐induced MR signal loss deviates from monoexponential decay, particularly at high b‐values (e.g., >1500 sec/mm2 for human brain tissues). A number of models have been developed to describe this anomalous diffusion behavior and relate the diffusion measurements to tissue structures. Recently, a new diffusion model was proposed by solving the Bloch‐Torrey equation using fractional order calculus with respect to time and space (Magin et al., J Magn Reson 2008;190:255‐270; Zhou et al., Proc Int'l Soc Magn Reson Med 2008). Using a spatial Laplacian ∇2β, this model yields a new set of parameters to describe anomalous diffusion: diffusion coefficient D, fractional order derivative in space β, and a spatial parameter μ (in units of μm). In this study, we demonstrate that the fractional calculus model can be successfully applied to analyzing diffusion images of healthy human brain tissues in vivo. Five human volunteers were scanned on a commercial 3‐T scanner using a customized single‐shot echo‐planar imaging diffusion sequence with 15 b values ranging from 0 to 4700 sec/mm2. The set of images was analyzed using the fractional calculus model, producing spatially resolved maps of D, β, and μ. The β and μ maps showed notable contrast between white and gray matter. The contrast has been attributed to the varying degree of complexity of the underlying tissue structures and microenvironment. Although the biophysical basis of β and μ remains elusive, the potential utility of these parameters to characterize the environment for molecular diffusion, as a complement to apparent diffusion coefficient, may lead to a new way to investigate tissue structural changes in disease progression, intervention, and regression. Magn Reson Med 63:562–569, 2010. © 2010 Wiley‐Liss, Inc. It is well known that diffusion-induced MR signal loss deviates from monoexponential decay, particularly at high b-values (e.g., >1500 sec/mm(2) for human brain tissues). A number of models have been developed to describe this anomalous diffusion behavior and relate the diffusion measurements to tissue structures. Recently, a new diffusion model was proposed by solving the Bloch-Torrey equation using fractional order calculus with respect to time and space (Magin et al., J Magn Reson 2008;190:255-270; Zhou et al., Proc Int'l Soc Magn Reson Med 2008). Using a spatial Laplacian [symbol: see text], this model yields a new set of parameters to describe anomalous diffusion: diffusion coefficient D, fractional order derivative in space beta, and a spatial parameter mu (in units of microm). In this study, we demonstrate that the fractional calculus model can be successfully applied to analyzing diffusion images of healthy human brain tissues in vivo. Five human volunteers were scanned on a commercial 3-T scanner using a customized single-shot echo-planar imaging diffusion sequence with 15 b values ranging from 0 to 4700 sec/mm(2). The set of images was analyzed using the fractional calculus model, producing spatially resolved maps of D, beta, and mu. The beta and mu maps showed notable contrast between white and gray matter. The contrast has been attributed to the varying degree of complexity of the underlying tissue structures and microenvironment. Although the biophysical basis of beta and mu remains elusive, the potential utility of these parameters to characterize the environment for molecular diffusion, as a complement to apparent diffusion coefficient, may lead to a new way to investigate tissue structural changes in disease progression, intervention, and regression.It is well known that diffusion-induced MR signal loss deviates from monoexponential decay, particularly at high b-values (e.g., >1500 sec/mm(2) for human brain tissues). A number of models have been developed to describe this anomalous diffusion behavior and relate the diffusion measurements to tissue structures. Recently, a new diffusion model was proposed by solving the Bloch-Torrey equation using fractional order calculus with respect to time and space (Magin et al., J Magn Reson 2008;190:255-270; Zhou et al., Proc Int'l Soc Magn Reson Med 2008). Using a spatial Laplacian [symbol: see text], this model yields a new set of parameters to describe anomalous diffusion: diffusion coefficient D, fractional order derivative in space beta, and a spatial parameter mu (in units of microm). In this study, we demonstrate that the fractional calculus model can be successfully applied to analyzing diffusion images of healthy human brain tissues in vivo. Five human volunteers were scanned on a commercial 3-T scanner using a customized single-shot echo-planar imaging diffusion sequence with 15 b values ranging from 0 to 4700 sec/mm(2). The set of images was analyzed using the fractional calculus model, producing spatially resolved maps of D, beta, and mu. The beta and mu maps showed notable contrast between white and gray matter. The contrast has been attributed to the varying degree of complexity of the underlying tissue structures and microenvironment. Although the biophysical basis of beta and mu remains elusive, the potential utility of these parameters to characterize the environment for molecular diffusion, as a complement to apparent diffusion coefficient, may lead to a new way to investigate tissue structural changes in disease progression, intervention, and regression. It is well known that diffusion-induced MR signal loss deviates from monoexponential decay, particularly at high b-values (e.g., >1500 sec/mm(2) for human brain tissues). A number of models have been developed to describe this anomalous diffusion behavior and relate the diffusion measurements to tissue structures. Recently, a new diffusion model was proposed by solving the Bloch-Torrey equation using fractional order calculus with respect to time and space (Magin et al., J Magn Reson 2008;190:255-270; Zhou et al., Proc Int'l Soc Magn Reson Med 2008). Using a spatial Laplacian [symbol: see text], this model yields a new set of parameters to describe anomalous diffusion: diffusion coefficient D, fractional order derivative in space beta, and a spatial parameter mu (in units of microm). In this study, we demonstrate that the fractional calculus model can be successfully applied to analyzing diffusion images of healthy human brain tissues in vivo. Five human volunteers were scanned on a commercial 3-T scanner using a customized single-shot echo-planar imaging diffusion sequence with 15 b values ranging from 0 to 4700 sec/mm(2). The set of images was analyzed using the fractional calculus model, producing spatially resolved maps of D, beta, and mu. The beta and mu maps showed notable contrast between white and gray matter. The contrast has been attributed to the varying degree of complexity of the underlying tissue structures and microenvironment. Although the biophysical basis of beta and mu remains elusive, the potential utility of these parameters to characterize the environment for molecular diffusion, as a complement to apparent diffusion coefficient, may lead to a new way to investigate tissue structural changes in disease progression, intervention, and regression. It is well known that diffusion-induced MR signal loss deviates from monoexponential decay, particularly at high b-values (e.g., >1500 sec/mm2 for human brain tissues). A number of models have been developed to describe this anomalous diffusion behavior and relate the diffusion measurements to tissue structures. Recently, a new diffusion model was proposed by solving the Bloch-Torrey equation using fractional order calculus with respect to time and space (Magin et al., J Magn Reson 2008; 190:255-270; Zhou et al., Proc Int'l Soc Magn Reson Med 2008). Using a spatial Laplacian {nabla}2 Delta *b, this model yields a new set of parameters to describe anomalous diffusion: diffusion coefficient D, fractional order derivative in space Delta *b, and a spatial parameter Delta *m (in units of Delta *mm). In this study, we demonstrate that the fractional calculus model can be successfully applied to analyzing diffusion images of healthy human brain tissues in vivo. Five human volunteers were scanned on a commercial 3-T scanner using a customized single-shot echo-planar imaging diffusion sequence with 15 b values ranging from 0 to 4700 sec/mm2. The set of images was analyzed using the fractional calculus model, producing spatially resolved maps of D, Delta *b, and Delta *m. The Delta *b and Delta *m maps showed notable contrast between white and gray matter. The contrast has been attributed to the varying degree of complexity of the underlying tissue structures and microenvironment. Although the biophysical basis of Delta *b and Delta *m remains elusive, the potential utility of these parameters to characterize the environment for molecular diffusion, as a complement to apparent diffusion coefficient, may lead to a new way to investigate tissue structural changes in disease progression, intervention, and regression. Magn Reson Med 63:562-569, 2010. [copy 2010 Wiley-Liss, Inc. |
Author | Magin, Richard L. Zhou, Xiaohong Joe Abdullah, Osama Gao, Qing |
Author_xml | – sequence: 1 givenname: Xiaohong Joe surname: Zhou fullname: Zhou, Xiaohong Joe email: xjzhou@uic.edu organization: Department of Radiology, University of Illinois Medical Center, Chicago, Illinois, USA – sequence: 2 givenname: Qing surname: Gao fullname: Gao, Qing organization: Department of Bioengineering, University of Illinois at Chicago, Chicago, Illinois, USA – sequence: 3 givenname: Osama surname: Abdullah fullname: Abdullah, Osama organization: Department of Bioengineering, University of Illinois at Chicago, Chicago, Illinois, USA – sequence: 4 givenname: Richard L. surname: Magin fullname: Magin, Richard L. organization: Department of Bioengineering, University of Illinois at Chicago, Chicago, Illinois, USA |
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References | Özarslan E, Basser PJ, Shepherd TM, Thelwall PE, Vemuri BC, Blackband SJ. Observation of anomalous diffusion in excised tissue by characterizing the diffusion-time dependence of the MR signal. J Magn Reson 2006; 183: 315-323. Sorensen AG, Buonanno FS, Gonzalez RG, Schwamm LH, Lev MH, Huang-Hellinger FR, Reese TG, Weisskoff RM, Davis TL, Suwanwela N, Can U, Moreira JA, Copen WA, Look RB, Finklestein SP, Rosen BR, Koroshetz WJ. Hyperacute stroke: evaluation with combined multisection diffusion-weighted and hemodynamically weighted echo-planar MR imaging. Radiology 1996; 199: 391-401. Hilfer R. Applications of fractional calculus in physics. Singapore: World Scientific; 2000, 472. Sehy JV, Zhao L, Xu JQ, Rayala HJ, Ackerman JJH, Neil JJ. Effects of physiologic challenge on the ADC of intracellular water in the Xenopus oocyte. Magn Reson Med 2004; 52: 239-247. Moseley ME, Cohen Y, Montorovitch J. Early detection of regional cerebral ischemia in cats: comparison of diffusion and T2 weighted MRI and spectroscopy. J Magn Reson 1990; 14: 330-346. Jensen JH, Helpern JA, Ramani A, Lu HZ, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 2005; 53: 1432-1440. Yablonskiy DA, Bretthorst GL, Ackerman JJH. Statistical model for diffusion attenuated MR signal. Magn Reson Med 2003; 50: 664-669. van Zijl PCM, Moonen CTW, Faustino P, Pekar J, Kaplan O, Cohen JS. Complete separation of intracellular and extracellular information in NMR spectra of perfused cells by diffusion weighted spectroscopy. Proc Natl Acad Sci U|S|A 1990; 88: 3228-3232. Hall MG, Barrick TR. From diffusion-weighted MRI to anomalous diffusion imaging. Magn Reson Med 2008; 59: 447-455. Pfeuffer J, Provencher S, Gruetter R. Water diffusion in rat brain in vivo as detected at very large b values is multicompartmental. MAGMA 1999; 8: 98-108. Sehy JV, Banks AA, Ackerman JJH, Neil JJ. Importance of intracellular water apparent diffusion to the measurement of membrane permeability. Biophys J 2002; 83: 2856-2863. Özarslan E, Basser PJ. MR diffusion-"diffraction" phenomenon in multi-pulse-field-gradient experiments. J Magn Reson 2007; 188: 285-294. Gao Q, Haldar JP, Rangwala N, Magin RL, Liang Z-P, Zhou XJ. Analysis of high b-value diffusion images using a fractional order diffusion model with denoising image reconstruction. Proc Int Soc Magn Reson Med 2009; 17: 1418. Magin RL, Abdullah O, Baleanu D, Zhou XJ. Anomalous diffusion expressed through fractional order differential operators in the Bloch-Torrey equation. J Magn Reson 2008; 190: 255-270. 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: 177-182. Carr HY, Purcell EM. Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys Rev 1954; 94: 630. Bennett KM, Schmainda KM, Bennett R, Rowe DB, Lu HB, Hyde JS. Characterization of continuously distributed cortical water diffusion rates with a stretched-exponential model. Magn Reson Med 2003; 50: 727-734. Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T, Okuda T, Liang L, Ge Y, Komohara Y, Ushio Y, Takahashi M. Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 1999; 9: 53-60. Le Bihan D. The "wet mind": water and functional neuroimaging. Phys Med Biol 2007; 52: R57-R90. Mulkern RV, Gudbjartsson H, Westin CF, Zengingonul HP, Gartner W, Guttmann CRG, Robertson RL, Kyriakos W, Schwartz R, Holtzman D, Jolesz FA, Maier SE. Multi-component apparent diffusion coefficients in human brain. NMR Biomed 1999; 12: 51-62. Inglis BA, Bossart EL, Buckley DL, Wirth ED, Mareci TH. Visualization of neural tissue water compartments using biexponential diffusion tensor MRI. Magn Reson Med 2001; 45: 580-587. Barboriak D. Imaging of brain tumors with diffusion-weighted and diffusion tensor MR imaging. Magn Reson Imaging Clin N Am 2003; 11: 379-401. Zhou XJ, Leeds NE, McKinnon GC, Kumar AJ. Characterization of benign and metastatic vertebral compression fractures with quantitative diffusion MR imaging. AJNR Am J Neuroradiol 2002; 23: 165-170. Sehy JV, Ackerman JJH, Neil JJ. Evidence that both fast and slow water ADC components arise from intracellular space. Magn Reson Med 2002; 48: 765-770. Clark CA, Hedehus M, Moseley ME. In vivo mapping of the fast and slow diffusion tensors in human brain. Magn Reson Med 2002; 47: 623-628. Clark CA, Le Bihan D. Water diffusion compartmentation and anisotropy at high b values in the human brain. Magn Reson Med 2000; 44: 852-859. Benveniste H, Hedlund LW, Johnson GA. Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke 1992; 23: 746-754. 2008; 190 1990; 14 2000; 44 2007; 188 2008; 59 2008 2007; 52 1999; 8 2001; 45 2003; 50 2003; 11 1999; 9 1999 2004; 52 2002; 47 1954; 94 2002; 48 1990; 88 2001 2000 2002; 83 2002; 23 1999; 12 2005; 53 2003; 49 1996; 199 2006; 183 1992; 23 2009; 17 |
References_xml | – reference: Clark CA, Le Bihan D. Water diffusion compartmentation and anisotropy at high b values in the human brain. Magn Reson Med 2000; 44: 852-859. – reference: Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T, Okuda T, Liang L, Ge Y, Komohara Y, Ushio Y, Takahashi M. Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 1999; 9: 53-60. – reference: Jensen JH, Helpern JA, Ramani A, Lu HZ, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 2005; 53: 1432-1440. – reference: Le Bihan D. The "wet mind": water and functional neuroimaging. Phys Med Biol 2007; 52: R57-R90. – reference: Hall MG, Barrick TR. From diffusion-weighted MRI to anomalous diffusion imaging. Magn Reson Med 2008; 59: 447-455. – reference: Hilfer R. Applications of fractional calculus in physics. Singapore: World Scientific; 2000, 472. – reference: van Zijl PCM, Moonen CTW, Faustino P, Pekar J, Kaplan O, Cohen JS. Complete separation of intracellular and extracellular information in NMR spectra of perfused cells by diffusion weighted spectroscopy. Proc Natl Acad Sci U|S|A 1990; 88: 3228-3232. – reference: Gao Q, Haldar JP, Rangwala N, Magin RL, Liang Z-P, Zhou XJ. Analysis of high b-value diffusion images using a fractional order diffusion model with denoising image reconstruction. Proc Int Soc Magn Reson Med 2009; 17: 1418. – reference: Barboriak D. Imaging of brain tumors with diffusion-weighted and diffusion tensor MR imaging. Magn Reson Imaging Clin N Am 2003; 11: 379-401. – reference: Sorensen AG, Buonanno FS, Gonzalez RG, Schwamm LH, Lev MH, Huang-Hellinger FR, Reese TG, Weisskoff RM, Davis TL, Suwanwela N, Can U, Moreira JA, Copen WA, Look RB, Finklestein SP, Rosen BR, Koroshetz WJ. Hyperacute stroke: evaluation with combined multisection diffusion-weighted and hemodynamically weighted echo-planar MR imaging. Radiology 1996; 199: 391-401. – reference: Özarslan E, Basser PJ, Shepherd TM, Thelwall PE, Vemuri BC, Blackband SJ. Observation of anomalous diffusion in excised tissue by characterizing the diffusion-time dependence of the MR signal. J Magn Reson 2006; 183: 315-323. – reference: Mulkern RV, Gudbjartsson H, Westin CF, Zengingonul HP, Gartner W, Guttmann CRG, Robertson RL, Kyriakos W, Schwartz R, Holtzman D, Jolesz FA, Maier SE. Multi-component apparent diffusion coefficients in human brain. NMR Biomed 1999; 12: 51-62. – reference: Benveniste H, Hedlund LW, Johnson GA. Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke 1992; 23: 746-754. – reference: 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: 177-182. – reference: Inglis BA, Bossart EL, Buckley DL, Wirth ED, Mareci TH. Visualization of neural tissue water compartments using biexponential diffusion tensor MRI. Magn Reson Med 2001; 45: 580-587. – reference: Pfeuffer J, Provencher S, Gruetter R. Water diffusion in rat brain in vivo as detected at very large b values is multicompartmental. MAGMA 1999; 8: 98-108. – reference: Özarslan E, Basser PJ. MR diffusion-"diffraction" phenomenon in multi-pulse-field-gradient experiments. J Magn Reson 2007; 188: 285-294. – reference: Sehy JV, Zhao L, Xu JQ, Rayala HJ, Ackerman JJH, Neil JJ. Effects of physiologic challenge on the ADC of intracellular water in the Xenopus oocyte. Magn Reson Med 2004; 52: 239-247. – reference: Zhou XJ, Leeds NE, McKinnon GC, Kumar AJ. Characterization of benign and metastatic vertebral compression fractures with quantitative diffusion MR imaging. AJNR Am J Neuroradiol 2002; 23: 165-170. – reference: Magin RL, Abdullah O, Baleanu D, Zhou XJ. Anomalous diffusion expressed through fractional order differential operators in the Bloch-Torrey equation. J Magn Reson 2008; 190: 255-270. – reference: Carr HY, Purcell EM. Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys Rev 1954; 94: 630. – reference: Sehy JV, Banks AA, Ackerman JJH, Neil JJ. Importance of intracellular water apparent diffusion to the measurement of membrane permeability. Biophys J 2002; 83: 2856-2863. – reference: Clark CA, Hedehus M, Moseley ME. In vivo mapping of the fast and slow diffusion tensors in human brain. Magn Reson Med 2002; 47: 623-628. – reference: Sehy JV, Ackerman JJH, Neil JJ. Evidence that both fast and slow water ADC components arise from intracellular space. Magn Reson Med 2002; 48: 765-770. – reference: Yablonskiy DA, Bretthorst GL, Ackerman JJH. Statistical model for diffusion attenuated MR signal. 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Snippet | It is well known that diffusion‐induced MR signal loss deviates from monoexponential decay, particularly at high b‐values (e.g., >1500 sec/mm2 for human brain... It is well known that diffusion-induced MR signal loss deviates from monoexponential decay, particularly at high b-values (e.g., >1500 sec/mm(2) for human... It is well known that diffusion-induced MR signal loss deviates from monoexponential decay, particularly at high b-values (e.g., >1500 sec/mm2 for human brain... |
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SubjectTerms | Algorithms anomalous diffusion Brain Brain - anatomy & histology Calculus Diffusion coefficient Diffusion Magnetic Resonance Imaging - methods diffusion model Echo-Planar Imaging - methods fractional order calculus high b value Humans Image Enhancement - methods Image Interpretation, Computer-Assisted - methods Mathematical models Microenvironments N.M.R Neuroimaging Reproducibility of Results Sensitivity and Specificity Substantia grisea |
Title | Studies of anomalous diffusion in the human brain using fractional order calculus |
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