Probing microscopic architecture of opaque heterogeneous systems using double-pulsed-field-gradient NMR.

Microarchitectural features of opaque porous media and biological tissues are of great importance in many scientific disciplines ranging from chemistry, material sciences, and geology to biology and medicine. Noninvasive characterization of coherently organized pores is rather straightforward since conventional diffusion magnetic resonance methods can detect anisotropy on a macroscopic scale; however, it remains extremely challenging to directly infer on microarchitectural features on the microscopic scale in heterogeneous porous media and biological cells that are comprised of randomly oriented compartments, a scenario widely encountered in Nature. Here, we show that the angular bipolar double-pulsed-field-gradient (bp-d-PFG) methodology is capable of reporting on unique microarchitectural features of highly heterogeneous systems. This was demonstrated on a toluene-in-water emulsion system, quartz sand, and even biological specimens such as yeast cells and isolated gray matter. We find that in the emulsion and yeast cells systems, the angular bp-d-PFG methodology uniquely revealed nearly an image of the pore space, since it conveyed direct microarchitectural information such as compartment shape and size. In two different quartz sand specimens, the angular bp-d-PFG experiments demonstrated the presence of randomly oriented anisotropic compartments. We also obtained unequivocal evidence that diffusion in interconnected interstices is restricted and therefore non-Gaussian. In biological contexts, the angular bp-d-PFG experiments could uniquely differentiate between spherical cells and randomly oriented compartments in gray matter tissue, information that could not be obtained by conventional NMR methods. The angular bp-d-PFG methodology also performs very well even when severe background gradients are present, as is often encountered in realistic systems. We conclude that this method seems to be the method of choice for characterizing the microstructure of porous media and biological cells noninvasively.

[1]  Evren Özarslan,et al.  Compartment shape anisotropy (CSA) revealed by double pulsed field gradient MR , 2009 .

[2]  Peter J Basser,et al.  The effect of the diffusion time and pulse gradient duration ratio on the diffraction pattern and the structural information estimated from q-space diffusion MR: experiments and simulations. , 2008, Journal of magnetic resonance.

[3]  Yoram Cohen,et al.  From single‐pulsed field gradient to double‐pulsed field gradient MR: gleaning new microstructural information and developing new forms of contrast in MRI , 2010, NMR in biomedicine.

[4]  D. Canet,et al.  Diffusive diffraction phenomenon in a porous polymer material observed by NMR using radio-frequency field gradients. , 2007, The Journal of chemical physics.

[5]  Simultaneous measurement of diffusion along multiple directions. , 2004, Journal of the American Chemical Society.

[6]  M. Koch,et al.  A tensor model and measures of microscopic anisotropy for double-wave-vector diffusion-weighting experiments with long mixing times. , 2010, Journal of magnetic resonance.

[7]  Peter J Basser,et al.  Observation of restricted diffusion in the presence of a free diffusion compartment: single- and double-PFG experiments. , 2009, Journal of magnetic resonance.

[8]  M. Johns,et al.  Characterisation of emulsion systems using NMR and MRI , 2007 .

[9]  D. Cory,et al.  Measurement of translational displacement probabilities by NMR: An indicator of compartmentation , 1990, Magnetic resonance in medicine.

[10]  Petrik Galvosas,et al.  Exploration of molecular dynamics during transient sorption of fluids in mesoporous materials , 2006, Nature.

[11]  Peter J Basser,et al.  Detecting diffusion-diffraction patterns in size distribution phantoms using double-pulsed field gradient NMR: Theory and experiments. , 2010, The Journal of chemical physics.

[12]  Y. Cohen,et al.  High b‐value q‐space analyzed diffusion‐weighted MRS and MRI in neuronal tissues – a technical review , 2002, NMR in biomedicine.

[13]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[14]  P. Basser,et al.  Observation of microscopic diffusion anisotropy in the spinal cord using double‐pulsed gradient spin echo MRI , 2008, Magnetic resonance in medicine.

[15]  D. Cory,et al.  Multiple Scattering by NMR , 1999 .

[16]  Jürgen Finsterbusch,et al.  Compartment size estimation with double wave vector diffusion‐weighted imaging , 2008, Magnetic resonance in medicine.

[17]  P J Basser,et al.  Detection of microscopic anisotropy in gray matter and in a novel tissue phantom using double Pulsed Gradient Spin Echo MR. , 2007, Journal of magnetic resonance.

[18]  Fernando Zelaya,et al.  High-resolution q-space imaging in porous structures , 1990 .

[19]  Dagmar van Dusschoten,et al.  Direct Observation of Fluid Mass Transfer Resistance in Porous Media by NMR Spectroscopy , 1998 .

[20]  J. V. van Duynhoven,et al.  Measurement of Oil Droplet Size Distributions in Food Oil/Water Emulsions by Time Domain Pulsed Field Gradient NMR. , 2001, Journal of colloid and interface science.

[21]  Bernhard Blümich,et al.  NMR Imaging of Materials , 2000 .

[22]  Mitra,et al.  Multiple wave-vector extensions of the NMR pulsed-field-gradient spin-echo diffusion measurement. , 1995, Physical review. B, Condensed matter.

[23]  P W Kuchel,et al.  NMR “diffusion‐diffraction” of water revealing alignment of erythrocytes in a magnetic field and their dimensions and membrane transport characteristics , 1997, Magnetic resonance in medicine.

[24]  Daniel Topgaard,et al.  Experimental determination of pore shape and size using q-space NMR microscopy in the long diffusion-time limit. , 2003, Magnetic resonance imaging.

[25]  Massimiliano Valentini,et al.  Diffusion NMR spectroscopy for the characterization of the size and interactions of colloidal matter: the case of vesicles and nanoparticles. , 2004, Journal of the American Chemical Society.

[26]  Paul T. Callaghan,et al.  Locally anisotropic motion in a macroscopically isotropic system: displacement correlations measured using double pulsed gradient spin‐echo NMR , 2002 .

[27]  V. Herold,et al.  Measurement of apparent cell radii using a multiple wave vector diffusion experiment , 2009, Magnetic resonance in medicine.

[28]  Karl G. Helmer,et al.  Restricted Diffusion in Sedimentary Rocks. Determination of Surface-Area-to-Volume Ratio and Surface Relaxivity , 1994 .

[29]  Dirk Demuth,et al.  NMR Studies of Single-File Diffusion in Unidimensional Channel Zeolites , 1996, Science.

[30]  P. Callaghan,et al.  Diffraction-like effects in NMR diffusion studies of fluids in porous solids , 1991, Nature.

[31]  Felix W. Wehrli,et al.  Quantifying axon diameter and intra-cellular volume fraction in excised mouse spinal cord with q-space imaging , 2010, NeuroImage.

[32]  Peter J Basser,et al.  Microscopic anisotropy revealed by NMR double pulsed field gradient experiments with arbitrary timing parameters. , 2008, The Journal of chemical physics.

[33]  Peter J Basser,et al.  Noninvasive bipolar double-pulsed-field-gradient NMR reveals signatures for pore size and shape in polydisperse, randomly oriented, inhomogeneous porous media. , 2010, The Journal of chemical physics.

[34]  Peter J Basser,et al.  Measuring small compartmental dimensions with low-q angular double-PGSE NMR: The effect of experimental parameters on signal decay. , 2009, Journal of magnetic resonance.

[35]  M. Prato,et al.  Diffusion-ordered NMR spectroscopy in the structural characterization of functionalized carbon nanotubes. , 2009, Journal of the American Chemical Society.

[36]  J. E. Tanner,et al.  Spin diffusion measurements : spin echoes in the presence of a time-dependent field gradient , 1965 .

[37]  Peter J Basser,et al.  A general framework to quantify the effect of restricted diffusion on the NMR signal with applications to double pulsed field gradient NMR experiments. , 2009, The Journal of chemical physics.

[38]  Jürgen Finsterbusch,et al.  Numerical simulation of double‐wave vector experiments investigating diffusion in randomly oriented ellipsoidal pores , 2009, Magnetic resonance in medicine.

[39]  J. Fraissard,et al.  129Xe NMR overview of xenon physisorbed in porous solids , 1999 .

[40]  Seungoh Ryu,et al.  Determining multiple length scales in rocks , 2000, Nature.

[41]  Timothy Edward John Behrens,et al.  Diffusion MRI : from quantitative measurement to in vivo neuroanatomy , 2014 .