Relationship between structural changes and hyperpolarized gas magnetic resonance imaging in chronic obstructive pulmonary disease using computational simulations with realistic alveolar geometry

Both the development of accurate models of lung function and their quantitative validation can be significantly enhanced by the use of functional imaging techniques. The advent of hyperpolarized noble gas magnetic resonance imaging (MRI) technology has increased the amount of local, functional information we can obtain from the lung. In particular, application of 3He to measure apparent diffusion coefficients has enabled some measure of lung microstructure and airspace size within the lung. Models mimicking image acquisition in hyperpolarized gas MRI can improve understanding of the relationship between image findings and lung structure, and can be used to improve the definition of imaging protocols. In this paper, we review the state of the art in hyperpolarized gas MRI modelling. We also present our own results, obtained using a Monte Carlo approach and a realistic alveolar sac geometry, which has previously been applied in functional lung studies. In this way, we demonstrate the potential for models combining lung function and image acquisition, which could provide valuable tools in both basic studies and clinical practice.

[1]  E. Miron,et al.  Polarization of the nuclear spins of noble-gas atoms by spin exchange with optically pumped alkali-metal atoms , 1984 .

[2]  Balthasar Eberle,et al.  Functional Evaluation of Emphysema Using Diffusion-Weighted 3Helium-Magnetic Resonance Imaging, High-Resolution Computed Tomography, and Lung Function Tests , 2004, Investigative radiology.

[3]  Sylvia Verbanck,et al.  Simulation of the apparent diffusion of helium-3 in the human acinus. , 2007, Journal of applied physiology.

[4]  X Wei,et al.  High equilibrium spin polarizations in solid 129Xe , 2000 .

[5]  A. Ingvarsson,et al.  Significance of lung hyperinflation in chronic obstructive pulmonary disease , 2007 .

[6]  John P. Mugler,et al.  Simulations of Short-Time Diffusivity in Lung Airspaces and Implications for S/V Measurements Using Hyperpolarized-Gas MRI , 2007, IEEE Transactions on Medical Imaging.

[7]  Dmitriy A Yablonskiy,et al.  Hyperpolarized 3He diffusion MRI and histology in pulmonary emphysema , 2006, Magnetic resonance in medicine.

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

[9]  William H. Press,et al.  Numerical recipes in C , 2002 .

[10]  Edwin J R van Beek,et al.  Quantitative analysis of regional airways obstruction using dynamic hyperpolarized 3He MRI—Preliminary results in children with cystic fibrosis , 2005, Journal of magnetic resonance imaging : JMRI.

[11]  Bastiaan Driehuys Hyperpolarized Gas MRI of the Lungs , 2009 .

[12]  Gary P. Zientara,et al.  Spin‐echoes for diffusion in bounded, heterogeneous media: A numerical study , 1980 .

[13]  Matthias Ochs,et al.  The number of alveoli in the human lung. , 2004, American journal of respiratory and critical care medicine.

[14]  R. Pauwels,et al.  Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: National Heart, Lung, and Blood Institute and World Health Organization Global Initiative for Chronic Obstructive Lung Disease (GOLD): executive summary. , 2001, Respiratory care.

[15]  Kevin R Minard,et al.  3D MRI of non-Gaussian (3)He gas diffusion in the rat lung. , 2007, Journal of magnetic resonance.

[16]  Ray F. Lee,et al.  Diffusional kurtosis imaging in the lung using hyperpolarized 3He , 2006, Magnetic resonance in medicine.

[17]  James R. Brookeman,et al.  Lung Air Spaces: MR Imaging Evaluation with , 1999 .

[18]  H. C. Torrey Bloch Equations with Diffusion Terms , 1956 .

[19]  Jim M. Wild,et al.  Feasibility of Image Registration and Intensity-Modulated Radiotherapy Planning With Hyperpolarized Helium-3 Magnetic Resonance Imaging for Non–Small-Cell Lung Cancer , 2007, International journal of radiation oncology, biology, physics.

[20]  Per Linse,et al.  The NMR Self-Diffusion Method Applied to Restricted Diffusion. Simulation of Echo Attenuation from Molecules in Spheres and between Planes , 1993 .

[21]  L W Hedlund,et al.  Spatially resolved measurements of hyperpolarized gas properties in the lung in vivo. Part I: Diffusion coefficient , 1999, Magnetic resonance in medicine.

[22]  P. Gevenois,et al.  Comparison of comcuted Density and Macroscopic Morphometry In Pu monary Emphysema , 1995 .

[23]  S. Newman,et al.  Radionuclide imaging technologies and their use in evaluating asthma drug deposition in the lungs. , 2003, Advanced drug delivery reviews.

[24]  Giles Santyr,et al.  Measurement of xenon diffusing capacity in the rat lung by hyperpolarized 129Xe MRI and dynamic spectroscopy in a single breath‐hold , 2006, Magnetic resonance in medicine.

[25]  E. Weibel Morphometry of the Human Lung , 1965, Springer Berlin Heidelberg.

[26]  John P Mugler,et al.  Evaluation of emphysema severity and progression in a rabbit model: comparison of hyperpolarized 3He and 129Xe diffusion MRI with lung morphometry. , 2007, Journal of applied physiology.

[27]  D E Olson,et al.  Physical models of the smaller pulmonary airways. , 1992, Journal of applied physiology.

[28]  A Potthast,et al.  Normal and abnormal pulmonary ventilation: visualization at hyperpolarized He-3 MR imaging. , 1996, Radiology.

[29]  Peter J. Hunter,et al.  Modeling RBC and Neutrophil Distribution Through an Anatomically Based Pulmonary Capillary Network , 2004, Annals of Biomedical Engineering.

[30]  Dmitriy A Yablonskiy,et al.  Quantitative in vivo assessment of lung microstructure at the alveolar level with hyperpolarized 3He diffusion MRI , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  F. Haas,et al.  Accuracy of pulmonary function tests in predicting exercise tolerance in chronic obstructive pulmonary disease. , 1984, Chest.

[32]  Eiichi Fukushima,et al.  A Multiple-Narrow-Pulse Approximation for Restricted Diffusion in a Time-Varying Field Gradient , 1996 .

[33]  A. Sukstanskii,et al.  In vivo lung morphometry with hyperpolarized 3He diffusion MRI: theoretical background. , 2008, Journal of magnetic resonance.

[34]  Janez Stepis Validity limits of Gaussian approximation in cumulant expansion for di!usion attenuation of spin echo , 1999 .

[35]  Dmitriy A Yablonskiy,et al.  Role of collateral paths in long-range diffusion in lungs. , 2008, Journal of applied physiology.

[36]  M Stampanoni,et al.  Finite element 3D reconstruction of the pulmonary acinus imaged by synchrotron X-ray tomography. , 2008, Journal of applied physiology.

[37]  Balthasar Eberle,et al.  Functional analysis in single-lung transplant recipients: a comparative study of high-resolution CT, 3He-MRI, and pulmonary function tests. , 2004, Chest.

[38]  L. W. Allen,et al.  99mTc technegas ventilation and perfusion lung scintigraphy for the diagnosis of pulmonary embolus. , 1999, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[39]  Yannick Crémillieux,et al.  Lung MRI for experimental drug research. , 2007, European journal of radiology.

[40]  E R Weibel,et al.  Pulmonary acinus: geometry and morphometry of the peripheral airway system in rat and rabbit. , 1987, The American journal of anatomy.

[41]  J E Hansen,et al.  Human air space shapes, sizes, areas, and volumes. , 1975, Journal of applied physiology.

[42]  Dmitriy A Yablonskiy,et al.  Effects of restricted diffusion on MR signal formation. , 2002, Journal of magnetic resonance.

[43]  Alan D. Lopez,et al.  Evidence-Based Health Policy--Lessons from the Global Burden of Disease Study , 1996, Science.

[44]  Schwartz,et al.  Short-time behavior of the diffusion coefficient as a geometrical probe of porous media. , 1993, Physical review. B, Condensed matter.

[45]  John P Mugler,et al.  Evaluation of asthma with hyperpolarized helium-3 MRI: correlation with clinical severity and spirometry. , 2006, Chest.

[46]  M. Bouchiat,et al.  Nuclear Polarization in He 3 Gas Induced by Optical Pumping and Dipolar Exchange , 1960 .

[47]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[48]  N Weiler,et al.  [Ultrafast MRI of lung ventilation using hyperpolarized helium-3]. , 2000, RoFo : Fortschritte auf dem Gebiete der Rontgenstrahlen und der Nuklearmedizin.

[49]  S. Hurd,et al.  Global Strategy for the Diagnosis, Management and Prevention of COPD: 2003 update , 2003, European Respiratory Journal.

[50]  D. Yablonskiy,et al.  MR imaging of diffusion of 3He gas in healthy and diseased lungs , 2000, Magnetic resonance in medicine.

[51]  Hans-Ulrich Kauczor,et al.  Assessment of lung ventilation by MR imaging: current status and future perspectives , 2002, European Radiology.

[52]  J R MacFall,et al.  Spatially resolved measurements of hyperpolarized gas properties in the lung in vivo. Part II: T∗︁2 , 1999, Magnetic resonance in medicine.

[53]  Alexander L Sukstanskii,et al.  Feasibility of diffusion-NMR surface-to-volume measurements tested by calculations and computer simulations. , 2004, Journal of magnetic resonance.

[54]  Callaghan,et al.  A simple matrix formalism for spin echo analysis of restricted diffusion under generalized gradient waveforms , 1997, Journal of magnetic resonance.

[55]  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.

[56]  V. Callot,et al.  Helium-3 MRI diffusion coefficient: correlation to morphometry in a model of mild emphysema , 2003, European Respiratory Journal.

[57]  R. Pauwels,et al.  Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) Workshop summary. , 2001, American journal of respiratory and critical care medicine.

[58]  William H. Press,et al.  Numerical recipes in C. The art of scientific computing , 1987 .

[59]  John P Mugler,et al.  Emphysema: hyperpolarized helium 3 diffusion MR imaging of the lungs compared with spirometric indexes--initial experience. , 2002, Radiology.

[60]  E R Weibel,et al.  Morphometry of the human pulmonary acinus , 1988, The Anatomical record.

[61]  Dmitriy A Yablonskiy,et al.  In vivo lung morphometry with hyperpolarized 3He diffusion MRI in canines with induced emphysema: disease progression and comparison with computed tomography. , 2007, Journal of applied physiology.

[62]  Eiichi Fukushima,et al.  Simple Solutions of the Torrey–Bloch Equations in the NMR Study of Molecular Diffusion , 1997 .

[63]  Jan Wolber,et al.  Characterization of diffusing capacity and perfusion of the rat lung in a lipopolysaccaride disease model using hyperpolarized 129Xe , 2003, Magnetic resonance in medicine.

[64]  Dmitriy A Yablonskiy,et al.  Magnetization tagging decay to measure long‐range 3He diffusion in healthy and emphysematous canine lungs , 2004, Magnetic resonance in medicine.

[65]  John P Mugler,et al.  Imaging the lungs in asthmatic patients by using hyperpolarized helium-3 magnetic resonance: assessment of response to methacholine and exercise challenge. , 2003, The Journal of allergy and clinical immunology.

[66]  Neil Woodhouse,et al.  Finite‐difference simulations of 3He diffusion in 3D alveolar ducts: Comparison with the “cylinder model” , 2004, Magnetic resonance in medicine.

[67]  Per Linse,et al.  The Validity of the Short-Gradient-Pulse Approximation in NMR Studies of Restricted Diffusion. Simulations of Molecules Diffusing between Planes, in Cylinders and Spheres , 1995 .

[68]  L W Hedlund,et al.  Postnatal growth and size of the pulmonary acinus and secondary lobule in man. , 1983, AJR. American journal of roentgenology.

[69]  F. Korosec,et al.  Functional lung imaging using hyperpolarized gas MRI , 2007, Journal of magnetic resonance imaging : JMRI.

[70]  H Itoh,et al.  Diffuse Lung Disease: Pathologic Basis for the High‐Resolution Computed Tomography Findings , 1993, Journal of thoracic imaging.

[71]  John P Mugler,et al.  Exploring lung function with hyperpolarized 129Xe nuclear magnetic resonance , 2004, Magnetic resonance in medicine.

[72]  A A Bankier,et al.  Pulmonary emphysema: subjective visual grading versus objective quantification with macroscopic morphometry and thin-section CT densitometry. , 1999, Radiology.

[73]  Janez Stepišnik,et al.  Validity limits of Gaussian approximation in cumulant expansion for diffusion attenuation of spin echo , 1999 .

[74]  Edwin J R van Beek,et al.  Investigating 3He diffusion NMR in the lungs using finite difference simulations and in vivo PGSE experiments. , 2004, Journal of magnetic resonance.

[75]  M Paiva,et al.  Model simulations of gas mixing and ventilation distribution in the human lung. , 1990, Journal of applied physiology.

[76]  Denis S. Grebenkov,et al.  NMR survey of reflected brownian motion , 2007 .

[77]  T A Altes,et al.  Hyperpolarized 3He MR lung ventilation imaging in asthmatics: Preliminary findings , 2001, Journal of magnetic resonance imaging : JMRI.

[78]  M. Rubens,et al.  Diffuse Lung Disease , 1990 .

[79]  John B. West,et al.  Respiratory Physiology - the Essentials , 1979 .

[80]  Lise Vejby Søgaard,et al.  Assessment of lung microstructure with magnetic resonance imaging of hyperpolarized Helium-3 , 2005, Respiratory Physiology & Neurobiology.

[81]  R Takaki,et al.  A three-dimensional model of the human pulmonary acinus. , 2000, Journal of applied physiology.

[82]  Edwin J R van Beek,et al.  Hyperpolarized 3-helium magnetic resonance imaging to probe lung function. , 2005, Proceedings of the American Thoracic Society.