In vivo preclinical cancer and tissue engineering applications of absolute oxygen imaging using pulse EPR.

The value of any measurement and a fortiori any measurement technology is defined by the reproducibility and the accuracy of the measurements. This implies a relative freedom of the measurement from factors confounding its accuracy. In the past, one of the reasons for the loss of focus on the importance of imaging oxygen in vivo was the difficulty in obtaining reproducible oxygen or pO2 images free from confounding variation. This review will briefly consider principles of electron paramagnetic oxygen imaging and describe how it achieves absolute oxygen measurements. We will provide a summary review of the progress in biomedical EPR imaging, predominantly in cancer biology research, discuss EPR oxygen imaging for cancer treatment and tissue graft assessment for regenerative medicine applications.

[1]  Thomas J Pohida,et al.  A new strategy for fast radiofrequency CW EPR imaging: direct detection with rapid scan and rotating gradients. , 2007, Journal of magnetic resonance.

[2]  Martyna Elas,et al.  Electron Paramagnetic Resonance Oxygen Images Correlate Spatially and Quantitatively with Oxylite Oxygen Measurements , 2006, Clinical Cancer Research.

[3]  Zhi-Pei Liang,et al.  Accelerated MR parameter mapping with low‐rank and sparsity constraints , 2015, Magnetic resonance in medicine.

[4]  Murali C Krishna,et al.  Electron paramagnetic resonance imaging of tumor hypoxia: Enhanced spatial and temporal resolution for in vivo pO2 determination , 2006, Magnetic resonance in medicine.

[5]  Colin Mailer,et al.  Absolute oxygen R1e imaging in vivo with pulse electron paramagnetic resonance , 2014, Magnetic resonance in medicine.

[6]  M. Simon,et al.  The role of oxygen availability in embryonic development and stem cell function , 2008, Nature Reviews Molecular Cell Biology.

[7]  Gareth R. Eaton,et al.  EPR IMAGING and IN VIVO EPR , 1991 .

[8]  D. Twieg The k-trajectory formulation of the NMR imaging process with applications in analysis and synthesis of imaging methods. , 1983, Medical physics.

[9]  Howard J Halpern,et al.  Imaging spin probe distribution in the tumor of a living mouse with 250 MHz EPR: Correlation with BOLD MRI , 2002, Magnetic resonance in medicine.

[10]  M. Kotecha Principles and Applications of Quantitative Parametric MRI in Tissue Engineering , 2017 .

[11]  P. Röschmann Radiofrequency penetration and absorption in the human body: limitations to high-field whole-body nuclear magnetic resonance imaging. , 1987, Medical physics.

[12]  Howard J Halpern,et al.  Electron paramagnetic resonance oxygen imaging of a rabbit tumor using localized spin probe delivery. , 2010, Medical physics.

[13]  Zhi-Pei Liang,et al.  Fast dynamic electron paramagnetic resonance (EPR) oxygen imaging using low-rank tensors. , 2016, Journal of magnetic resonance.

[14]  Andrew G. Taube,et al.  Single‐point (constant‐time) imaging in radiofrequency Fourier transform electron paramagnetic resonance † , 2002, Magnetic resonance in medicine.

[15]  S. Cherry,et al.  MicroPET II: design, development and initial performance of an improved microPET scanner for small-animal imaging. , 2003, Physics in medicine and biology.

[16]  Howard J Halpern,et al.  Characterization of response to radiation mediated gene therapy by means of multimodality imaging , 2009, Magnetic resonance in medicine.

[17]  Martyna Elas,et al.  Quantitative tumor oxymetric images from 4D electron paramagnetic resonance imaging (EPRI): Methodology and comparison with blood oxygen level‐dependent (BOLD) MRI , 2003, Magnetic resonance in medicine.

[18]  Howard J Halpern,et al.  Comparison of local and global angular interpolation applied to spectral-spatial EPR image reconstruction. , 2007, Medical physics.

[19]  James B. Mitchell,et al.  Low-field magnetic resonance imaging to visualize chronic and cycling hypoxia in tumor-bearing mice. , 2010, Cancer research.

[20]  C. Ricordi,et al.  Influence of In Vitro and In Vivo Oxygen Modulation on β Cell Differentiation From Human Embryonic Stem Cells , 2014, Stem cells translational medicine.

[21]  J S Petersson,et al.  EPR and DNP properties of certain novel single electron contrast agents intended for oximetric imaging. , 1998, Journal of magnetic resonance.

[22]  Shingo Matsumoto,et al.  Antiangiogenic agent sunitinib transiently increases tumor oxygenation and suppresses cycling hypoxia. , 2011, Cancer research.

[23]  Mark W. Dewhirst,et al.  Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response , 2008, Nature Reviews Cancer.

[24]  James B. Mitchell,et al.  Overhauser enhanced magnetic resonance imaging for tumor oximetry: Coregistration of tumor anatomy and tissue oxygen concentration , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Welch,et al.  PET imaging of hypoxia. , 2001, The quarterly journal of nuclear medicine : official publication of the Italian Association of Nuclear Medicine (AIMN) [and] the International Association of Radiopharmacology.

[26]  K A Athanasiou,et al.  Hypoxic chondrogenic differentiation of human embryonic stem cells enhances cartilage protein synthesis and biomechanical functionality. , 2008, Osteoarthritis and cartilage.

[27]  James B. Mitchell,et al.  Transient decrease in tumor oxygenation after intravenous administration of pyruvate , 2012, Magnetic resonance in medicine.

[28]  H. Fujii,et al.  Development and testing of a CW-EPR apparatus for imaging of short-lifetime nitroxyl radicals in mouse head. , 2008, Journal of magnetic resonance.

[29]  C. Pelizzari,et al.  Magnet and gradient coil system for low-field EPR imaging , 2002 .

[30]  Bo Chen,et al.  Stem Cell Tissue Engineering and Regenerative Medicine , 2017 .

[31]  Angelique M. Nelson,et al.  Hypoxia induces re‐entry of committed cells into pluripotency , 2013, Stem cells.

[32]  M. Mehring,et al.  High resolution ESR imaging , 1986 .

[33]  Chad R. Haney,et al.  Where It’s at Really Matters: In Situ In Vivo Vascular Endothelial Growth Factor Spatially Correlates with Electron Paramagnetic Resonance pO2 Images in Tumors of Living Mice , 2010, Molecular Imaging and Biology.

[34]  Howard J. Halpern,et al.  Imaging radio frequency electron‐spin‐resonance spectrometer with high resolution and sensitivity for in vivo measurements , 1989 .

[35]  J. Zweier,et al.  Noninvasive measurement of anatomic structure and intraluminal oxygenation in the gastrointestinal tract of living mice with spatial and spectral EPR imaging. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[36]  S. Ljunggren A simple graphical representation of fourier-based imaging methods , 1983 .

[37]  Colin Mailer,et al.  A Versatile High Speed 250 MHz Pulse Imager for Biomedical Applications. , 2008, Concepts in magnetic resonance. Part B, Magnetic resonance engineering.

[38]  H. Halpern,et al.  Comparison of pulse sequences for R1-based electron paramagnetic resonance oxygen imaging. , 2015, Journal of magnetic resonance.

[39]  J. Zweier,et al.  In vivo measurement of arterial and venous oxygenation in the rat using 3D spectral-spatial electron paramagnetic resonance imaging. , 1998, Physics in medicine and biology.

[40]  Martyna Elas,et al.  Electron paramagnetic resonance oxygen image hypoxic fraction plus radiation dose strongly correlates with tumor cure in FSa fibrosarcomas. , 2008, International journal of radiation oncology, biology, physics.

[41]  P. Kuppusamy,et al.  In vivo imaging of changes in tumor oxygenation during growth and after treatment , 2007, Magnetic resonance in medicine.

[42]  H. Halpern,et al.  In Vivo EPR Oxygen Imaging , 2017 .

[43]  Cato T Laurencin,et al.  Optimally porous and biomechanically compatible scaffolds for large-area bone regeneration. , 2012, Tissue engineering. Part A.

[44]  S. Cherry,et al.  High-resolution PET detector design: modelling components of intrinsic spatial resolution , 2005, Physics in medicine and biology.

[45]  Colin Mailer,et al.  Spin echo spectroscopic electron paramagnetic resonance imaging , 2006, Magnetic resonance in medicine.

[46]  James B. Mitchell,et al.  Strategies for improved temporal and spectral resolution in in vivo oximetric imaging using time‐domain EPR , 2007, Magnetic resonance in medicine.

[47]  H. Degani,et al.  Magnetic resonance imaging of tumor vasculature , 2003, Thrombosis and Haemostasis.

[48]  Colin Mailer,et al.  Comparison of 250 MHz electron spin echo and continuous wave oxygen EPR imaging methods for in vivo applications. , 2011, Medical physics.

[49]  Sankaran Subramanian,et al.  Radiofrequency FT EPR Spectroscopy and Imaging , 1993 .

[50]  Howard J Halpern,et al.  Spatially uniform sampling in 4-D EPR spectral-spatial imaging. , 2007, Journal of magnetic resonance.

[51]  James B. Mitchell,et al.  Maximum Entropy Reconstruction Methods in Electron Paramagnetic Resonance Imaging , 2003, Ann. Oper. Res..

[52]  Alfredo Quiñones-Hinojosa,et al.  Oxygen in stem cell biology: a critical component of the stem cell niche. , 2010, Cell stem cell.

[53]  Howard J Halpern,et al.  Principal component analysis enhances SNR for dynamic electron paramagnetic resonance oxygen imaging of cycling hypoxia in vivo , 2014, Magnetic resonance in medicine.

[54]  Howard J Halpern,et al.  Immobilization Using Dental Material Casts Facilitates Accurate Serial and Multimodality Small Animal Imaging. , 2008, Concepts in magnetic resonance. Part B, Magnetic resonance engineering.

[55]  J. Vacanti,et al.  Tissue engineering : Frontiers in biotechnology , 1993 .

[56]  E. Place,et al.  Complexity in biomaterials for tissue engineering. , 2009, Nature materials.

[57]  S. Emid,et al.  High resolution NMR imaging in solids , 1985 .