Tomographic phase microscopy: principles and applications in bioimaging [Invited].

Tomographic phase microscopy (TPM) is an emerging optical microscopic technique for bioimaging. TPM uses digital holographic measurements of complex scattered fields to reconstruct three-dimensional refractive index (RI) maps of cells with diffraction-limited resolution by solving inverse scattering problems. In this paper, we review the developments of TPM from the fundamental physics to its applications in bioimaging. We first provide a comprehensive description of the tomographic reconstruction physical models used in TPM. The RI map reconstruction algorithms and various regularization methods are discussed. Selected TPM applications for cellular imaging, particularly in hematology, are reviewed. Finally, we examine the limitations of current TPM systems, propose future solutions, and envision promising directions in biomedical research.

[1]  M. Gu,et al.  Principles Of Three-Dimensional Imaging In Confocal Microscopes , 1996 .

[2]  Minh N. Do,et al.  Visualizing Escherichia coli Sub-Cellular Structure Using Sparse Deconvolution Spatial Light Interference Tomography , 2012, PloS one.

[3]  Yongjin Sung,et al.  Video-rate tomographic phase microscopy. , 2011, Journal of biomedical optics.

[4]  Jing-Wei Su,et al.  Tomographic diffractive microscopy of living cells based on a common-path configuration. , 2014, Optics letters.

[5]  L Hesselink,et al.  High speed optical tomography for flow visualization. , 1985, Applied optics.

[6]  C. Fang-Yen,et al.  Optical diffraction tomography for high resolution live cell imaging. , 2009, Optics express.

[7]  Subra Suresh,et al.  The biomechanics toolbox: experimental approaches for living cells and biomolecules , 2003 .

[8]  J. Gall,et al.  Cajal bodies, nucleoli, and speckles in the Xenopus oocyte nucleus have a low-density, sponge-like structure. , 2004, Molecular biology of the cell.

[9]  Pietro Ferraro,et al.  Dynamic DIC by digital holography microscopy for enhancing phase-contrast visualization , 2011, Biomedical optics express.

[10]  D Zicha,et al.  Phase-shifting interference microscopy applied to the analysis of cell behaviour. , 1993, Symposia of the Society for Experimental Biology.

[11]  R. W. Lawrence,et al.  Digital Image Formation From Electronically Detected Holograms , 1967 .

[12]  P. Marquet,et al.  Marker-free phase nanoscopy , 2013, Nature Photonics.

[13]  YongKeun Park,et al.  Measurements of morphological and biochemical alterations in individual neuron cells associated with early neurotoxic effects in Parkinson’s disease , 2016, bioRxiv.

[14]  Zhuo Wang,et al.  Tissue refractive index as marker of disease. , 2011, Journal of biomedical optics.

[15]  Yongjin Sung,et al.  Stain-Free Quantification of Chromosomes in Live Cells Using Regularized Tomographic Phase Microscopy , 2012, PloS one.

[16]  S. Kou,et al.  Image formation in holographic tomography: high-aperture imaging conditions. , 2009, Applied optics.

[17]  N. Mohandas,et al.  Red cell membrane: past, present, and future. , 2008, Blood.

[18]  A. Khintchine Korrelationstheorie der stationären stochastischen Prozesse , 1934 .

[19]  Yongjin Sung,et al.  Deterministic regularization of three-dimensional optical diffraction tomography. , 2011, Journal of the Optical Society of America. A, Optics, image science, and vision.

[20]  Wonshik Choi,et al.  Full-field and single-shot quantitative phase microscopy using dynamic speckle illumination. , 2011, Optics letters.

[21]  D. Agard,et al.  Fluorescence microscopy in three dimensions. , 1989, Methods in cell biology.

[22]  Anthony J. Devaney,et al.  Phase-retrieval and intensity-only reconstruction algorithms for optical diffraction tomography , 1993 .

[23]  Sung-Hee Hong,et al.  Characterizations of individual mouse red blood cells parasitized by Babesia microti using 3-D holographic microscopy , 2015, Scientific Reports.

[24]  Joseph A. Izatt,et al.  Refractive index tomography with structured illumination , 2017, 1702.03595.

[25]  Kyoohyun Kim,et al.  Three-dimensional label-free imaging and quantification of lipid droplets in live hepatocytes , 2016, Scientific Reports.

[26]  Gabriel Popescu,et al.  Fourier phase microscopy for investigation of biological structures and dynamics. , 2004, Optics letters.

[27]  Michael Unser,et al.  An Introduction to Sparse Stochastic Processes , 2014 .

[28]  Yutaka Yamashita,et al.  Label-free imaging of intracellular motility by low-coherent quantitative phase microscope in reflection geometry , 2011, International Conference on Optical Instruments and Technology.

[29]  Malgorzata Kujawinska,et al.  Active limited-angle tomographic phase microscope , 2015, Journal of biomedical optics.

[30]  Joseph M. Martel,et al.  Three-Dimensional Holographic Refractive-Index Measurement of Continuously Flowing Cells in a Microfluidic Channel. , 2014, Physical review applied.

[31]  Vadim Backman,et al.  Microscopic imaging and spectroscopy with scattered light. , 2010, Annual review of biomedical engineering.

[32]  Patrick L. Combettes,et al.  An Algorithm for Splitting Parallel Sums of Linearly Composed Monotone Operators, with Applications to Signal Recovery , 2013, 1305.5828.

[33]  A. Devaney Inverse-scattering theory within the Rytov approximation. , 1981, Optics letters.

[34]  Gabriel Popescu,et al.  Quantitative phase imaging for medical diagnosis , 2017, Journal of biophotonics.

[35]  Jean-Jacques Delaunay,et al.  Improved and isotropic resolution in tomographic diffractive microscopy combining sample and illumination rotation , 2011 .

[36]  YongKeun Park,et al.  Three-dimensional refractive index tomograms and deformability of individual human red blood cells from cord blood of newborn infants and maternal blood , 2015, Journal of biomedical optics.

[37]  Pilhan Kim,et al.  Holographic intravital microscopy for 2-D and 3-D imaging intact circulating blood cells in microcapillaries of live mice , 2016, Scientific Reports.

[38]  Michael Unser,et al.  Learning approach to optical tomography , 2015, 1502.01914.

[39]  Paul Lagasse,et al.  Beam-propagation method: analysis and assessment , 1981 .

[40]  Zhuo Wang,et al.  Optical measurement of cycle-dependent cell growth , 2011, Proceedings of the National Academy of Sciences.

[41]  Gabriel Popescu,et al.  Hilbert phase microscopy for investigating fast dynamics in transparent systems. , 2005, Optics letters.

[42]  G. Popescu,et al.  Inverse scattering solutions using low-coherence light. , 2014, Optics letters.

[43]  M. Gustafsson,et al.  Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. , 2008, Biophysical journal.

[44]  Radim Chmelík,et al.  Coherence-controlled holographic microscope , 2010, Polish-Slovak-Czech Optical Conference on Wave and Quantum Aspects of Contemporary Optics.

[45]  Natan T. Shaked,et al.  Rapid 3D Refractive‐Index Imaging of Live Cells in Suspension without Labeling Using Dielectrophoretic Cell Rotation , 2016, Advanced science.

[46]  S. Chien Red cell deformability and its relevance to blood flow. , 1987, Annual review of physiology.

[47]  Jonghee Yoon,et al.  Optical diffraction tomography using a digital micromirror device for stable measurements of 4D refractive index tomography of cells , 2016, SPIE BiOS.

[48]  Robert G. Parton,et al.  Opinion: Lipid droplets: a unified view of a dynamic organelle , 2006, Nature Reviews Molecular Cell Biology.

[49]  Radim Chmelik,et al.  Quantitative phase imaging through scattering media by means of coherence-controlled holographic microscope , 2015, Journal of biomedical optics.

[50]  Demetri Psaltis,et al.  Optical Tomographic Image Reconstruction Based on Beam Propagation and Sparse Regularization , 2016, IEEE Transactions on Computational Imaging.

[51]  Aggelos K. Katsaggelos,et al.  Sparse Bayesian image restoration , 2010, 2010 IEEE International Conference on Image Processing.

[52]  Full-field Interferometric Confocal Microscopy using a VCSEL Array , 2014 .

[53]  Gabriel Popescu,et al.  Solving inverse scattering problems in biological samples by quantitative phase imaging , 2016 .

[54]  Philippe Andrey,et al.  A generic classification-based method for segmentation of nuclei in 3D images of early embryos , 2014, BMC Bioinformatics.

[55]  Yongjin Sung,et al.  Multiple Phases of Chondrocyte Enlargement Underlie Differences in Skeletal Proportions , 2013, Nature.

[56]  Colin J. R. Sheppard,et al.  Three-dimensional coherent transfer function in a reflection-mode confocal scanning microscope , 1991 .

[57]  C. Fang-Yen,et al.  Tomographic phase microscopy , 2008, Nature Methods.

[58]  A. Lohmann,et al.  Complex spatial filtering with binary masks. , 1966, Applied optics.

[59]  M. Kirschner,et al.  Size homeostasis in adherent cells studied by synthetic phase microscopy , 2013, Proceedings of the National Academy of Sciences.

[60]  T. Kozacki,et al.  Investigation of limitations of optical diffraction tomography , 2007 .

[61]  YongKeun Park,et al.  Hyperspectral optical diffraction tomography. , 2016, Optics express.

[62]  Sang Yun Lee,et al.  The Effects of Ethanol on the Morphological and Biochemical Properties of Individual Human Red Blood Cells , 2015, PloS one.

[63]  Laura Waller,et al.  Computational imaging: Machine learning for 3D microscopy , 2015, Nature.

[64]  H. Meiselman,et al.  Geometry of Neonatal and Adult Red Blood Cells , 1983, Pediatric Research.

[65]  Tan H. Nguyen,et al.  Diffraction phase microscopy: principles and applications in materials and life sciences , 2014 .

[66]  Mike Tyers,et al.  How Cells Coordinate Growth and Division , 2004, Current Biology.

[67]  Marc Teboulle,et al.  Fast Gradient-Based Algorithms for Constrained Total Variation Image Denoising and Deblurring Problems , 2009, IEEE Transactions on Image Processing.

[68]  Subra Suresh,et al.  Cellular normoxic biophysical markers of hydroxyurea treatment in sickle cell disease , 2016, Proceedings of the National Academy of Sciences.

[69]  YongKeun Park,et al.  Active illumination using a digital micromirror device for quantitative phase imaging. , 2015, Optics letters.

[70]  Stuart Crozier,et al.  Image registration guided, sparsity constrained reconstructions for dynamic MRI. , 2014, Magnetic resonance imaging.

[71]  Michel Barlaud,et al.  Deterministic edge-preserving regularization in computed imaging , 1997, IEEE Trans. Image Process..

[72]  B. Kemper,et al.  Digital holographic microscopy for live cell applications and technical inspection. , 2008, Applied optics.

[73]  Jing-Wei Su,et al.  Investigating the backscattering characteristics of individual normal and cancerous cells based on experimentally determined three-dimensional refractive index distributions , 2012, Photonics Asia.

[74]  Mor Habaza,et al.  Tomographic phase microscopy with 180° rotation of live cells in suspension by holographic optical tweezers. , 2015, Optics letters.

[75]  A P Dhawan,et al.  Algorithms for limited-view computed tomography: an annotated bibliography and a challenge. , 1985, Applied optics.

[76]  R. Barer,et al.  Refractive Index of Concentrated Protein Solutions , 1954, Nature.

[77]  YongKeun Park,et al.  Profiling individual human red blood cells using common-path diffraction optical tomography , 2014, Scientific Reports.

[78]  L. Rudin,et al.  Nonlinear total variation based noise removal algorithms , 1992 .

[79]  Yongjin Sung,et al.  Assessing light scattering of intracellular organelles in single intact living cells. , 2009, Optics express.

[80]  Kyoohyun Kim,et al.  Synthetic Fourier transform light scattering. , 2013, Optics express.

[81]  Michael G. Somekh,et al.  Wide field amplitude and phase confocal microscope with speckle illumination , 2000 .

[82]  Tan H. Nguyen,et al.  Plane-wave decomposition of spatially random fields. , 2015, Optics letters.

[83]  E. Cuche,et al.  Digital holography for quantitative phase-contrast imaging. , 1999, Optics letters.

[84]  S. D. Babacan,et al.  White-light diffraction tomography of unlabelled live cells , 2014, Nature Photonics.

[85]  Laura Waller,et al.  Video-rate processing in tomographic phase microscopy of biological cells using CUDA. , 2016, Optics express.

[86]  Andreas Stemmer,et al.  Simplified approach to diffraction tomography in optical microscopy. , 2009, Optics express.

[87]  Sophie G. Martin,et al.  Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle , 2009, Nature.

[88]  YongKeun Park,et al.  Simultaneous 3D visualization and position tracking of optically trapped particles using optical diffraction tomography , 2015 .

[89]  Gabriel Popescu,et al.  Synthetic aperture tomographic phase microscopy for 3D imaging of live cells in translational motion. , 2008, Optics express.

[90]  W. Lewis,et al.  Surface/Volume Ratio: Implications for Phytoplankton Morphology , 1976, Science.

[91]  Zhiqiang Chen,et al.  Anisotropic total variation for limited-angle CT reconstruction , 2010, IEEE Nuclear Science Symposuim & Medical Imaging Conference.

[92]  Julie A. Theriot,et al.  Mechanism of shape determination in motile cells , 2008, Nature.

[93]  A. J. Devaney,et al.  A Computer Simulation Study of Diffraction Tomography , 1983, IEEE Transactions on Biomedical Engineering.

[94]  S. Suresh,et al.  Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum , 2007, Proceedings of the National Academy of Sciences.

[95]  Chao Zuo,et al.  Lensless phase microscopy and diffraction tomography with multi-angle and multi-wavelength illuminations using a LED matrix. , 2015, Optics express.

[96]  F. Zernike Phase contrast, a new method for the microscopic observation of transparent objects , 1942 .

[97]  V. Ntziachristos Fluorescence molecular imaging. , 2006, Annual review of biomedical engineering.

[98]  Zahid Yaqoob,et al.  Single-shot Full-field reflection phase microscopy , 2011, Optics express.

[99]  Kyoohyun Kim,et al.  Optical diffraction tomography techniques for the study of cell pathophysiology , 2016, 1603.00592.

[100]  Hong Yan,et al.  An improved algorithm for rotational motion artifact suppression in MRI , 1998, IEEE Transactions on Medical Imaging.

[101]  Emmanuel J. Candès,et al.  Robust uncertainty principles: exact signal reconstruction from highly incomplete frequency information , 2004, IEEE Transactions on Information Theory.

[102]  E. Cuche,et al.  Simultaneous amplitude-contrast and quantitative phase-contrast microscopy by numerical reconstruction of Fresnel off-axis holograms. , 1999, Applied optics.

[103]  YongKeun Park,et al.  Biomedical applications of holographic microspectroscopy [invited]. , 2014, Applied optics.

[104]  R. Coleman,et al.  The role of lipid droplets in metabolic disease in rodents and humans. , 2011, The Journal of clinical investigation.

[105]  P. So,et al.  Scanning color optical tomography (SCOT). , 2015, Optics express.

[106]  Piotr Makowski,et al.  Generalized total variation iterative constraint strategy in limited angle optical diffraction tomography. , 2016, Optics express.

[107]  Yoram Bresler,et al.  Globally convergent edge-preserving regularized reconstruction: an application to limited-angle tomography , 1998, IEEE Trans. Image Process..

[108]  Kyoohyun Kim,et al.  High-Resolution 3-D Refractive Index Tomography and 2-D Synthetic Aperture Imaging of Live Phytoplankton , 2014 .

[109]  Björn Kemper,et al.  Tomographic phase microscopy of living three-dimensional cell cultures , 2014, Journal of biomedical optics.

[110]  Subra Suresh,et al.  Biophysics of Malarial Parasite Exit from Infected Erythrocytes , 2011, PloS one.

[111]  Hamed Hamid Muhammed,et al.  New Approach for Limited-Angle Problems in Electron Microscope Based on Compressed Sensing , 2013 .

[112]  Paul Nurse,et al.  A spatial gradient coordinates cell size and mitotic entry in fission yeast , 2009, Nature.

[113]  O. Haeberlé,et al.  Tomographic diffractive microscopy: basics, techniques and perspectives , 2010 .

[114]  YongKeun Park,et al.  High-resolution three-dimensional imaging of red blood cells parasitized by Plasmodium falciparum and in situ hemozoin crystals using optical diffraction tomography , 2013, Journal of biomedical optics.

[115]  SangYun Lee,et al.  Refractive index tomograms and dynamic membrane fluctuations of red blood cells from patients with diabetes mellitus , 2017 .

[116]  Kyoohyun Kim,et al.  Label-free characterization of white blood cells by measuring 3D refractive index maps. , 2015, Biomedical optics express.

[117]  N. Wiener Generalized harmonic analysis , 1930 .

[118]  Marie Louise Groot,et al.  Short-coherence off-axis holographic phase microscopy of live cell dynamics , 2012, Biomedical optics express.

[119]  R. Barer Interference Microscopy and Mass Determination , 1952, Nature.

[120]  L. Tian,et al.  3D intensity and phase imaging from light field measurements in an LED array microscope , 2015 .

[121]  G. Popescu Quantitative Phase Imaging of Cells and Tissues , 2011 .

[122]  Jong Chul Ye,et al.  Comparative study of iterative reconstruction algorithms for missing cone problems in optical diffraction tomography. , 2015, Optics express.

[123]  Wong Cheng Lee,et al.  Multivariate biophysical markers predictive of mesenchymal stromal cell multipotency , 2014, Proceedings of the National Academy of Sciences.

[124]  Yongkeun Park,et al.  Refractive index maps and membrane dynamics of human red blood cells parasitized by Plasmodium falciparum , 2008, Proceedings of the National Academy of Sciences.

[125]  J. Schuman,et al.  Optical coherence tomography. , 2000, Science.

[126]  P. Brown,et al.  On the distribution of protein refractive index increments. , 2011, Biophysical journal.

[127]  Jing-Wei Su,et al.  Digital holographic microtomography for high‐resolution refractive index mapping of live cells , 2013, Journal of biophotonics.

[128]  Frederic Noo,et al.  A local shift-variant Fourier model and experimental validation of circular cone-beam computed tomography artifacts. , 2009, Medical physics.

[129]  Zahid Yaqoob,et al.  Dynamic speckle illumination wide-field reflection phase microscopy. , 2014, Optics letters.

[130]  Ogobara K. Doumbo,et al.  The pathogenic basis of malaria , 2002, Nature.

[131]  Leann Tilley,et al.  Illuminating Plasmodium falciparum-infected red blood cells. , 2007, Trends in parasitology.

[132]  P. So,et al.  Modeling the depth-sectioning effect in reflection-mode dynamic speckle-field interferometric microscopy. , 2017, Optics express.

[133]  E. Wolf Three-dimensional structure determination of semi-transparent objects from holographic data , 1969 .

[134]  E. Cuche,et al.  Cell refractive index tomography by digital holographic microscopy. , 2006, Optics letters.

[135]  D Zicha,et al.  Rapid, microtubule-dependent fluctuations of the cell margin. , 1997, Journal of cell science.