Quantitative phase imaging in biomedicine

Quantitative phase imaging (QPI) has emerged as a valuable method for investigating cells and tissues. QPI operates on unlabelled specimens and, as such, is complementary to established fluorescence microscopy, exhibiting lower phototoxicity and no photobleaching. As the images represent quantitative maps of optical path length delays introduced by the specimen, QPI provides an objective measure of morphology and dynamics, free of variability due to contrast agents. Owing to the tremendous progress witnessed especially in the past 10–15 years, a number of technologies have become sufficiently reliable and translated to biomedical laboratories. Commercialization efforts are under way and, as a result, the QPI field is now transitioning from a technology-development-driven to an application-focused field. In this Review, we aim to provide a critical and objective overview of this dynamic research field by presenting the scientific context, main principles of operation and current biomedical applications.Over the past 10–15 years, quantitative phase imaging has moved from a research-driven to an application-focused field. This Review presents the main principles of operation and representative basic and clinical science applications.

[1]  William H. Grover,et al.  Using buoyant mass to measure the growth of single cells , 2010, Nature Methods.

[2]  Kieran G Larkin,et al.  Mapping optical path length and image enhancement using quantitative orientation-independent differential interference contrast microscopy , 2017, Journal of biomedical optics.

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

[4]  George Lee,et al.  Image analysis and machine learning in digital pathology: Challenges and opportunities , 2016, Medical Image Anal..

[5]  Christian Depeursinge,et al.  Determination of Transmembrane Water Fluxes in Neurons Elicited by Glutamate Ionotropic Receptors and by the Cotransporters KCC2 and NKCC1: A Digital Holographic Microscopy Study , 2011, The Journal of Neuroscience.

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

[7]  Gabriel Popescu,et al.  Observation of dynamic subdomains in red blood cells. , 2006, Journal of biomedical optics.

[8]  Takeo Kanade,et al.  Understanding the phase contrast optics to restore artifact-free microscopy images for segmentation , 2012, Medical Image Anal..

[9]  C K Hitzenberger,et al.  Differential phase contrast in optical coherence tomography. , 1999, Optics letters.

[10]  Pierre Marquet,et al.  Review of quantitative phase-digital holographic microscopy: promising novel imaging technique to resolve neuronal network activity and identify cellular biomarkers of psychiatric disorders , 2014, Neurophotonics.

[11]  G. Ripandelli,et al.  Optical coherence tomography. , 1998, Seminars in ophthalmology.

[12]  R. Horstmeyer,et al.  Diffraction tomography with Fourier ptychography. , 2015, Optica.

[13]  Gabriel Popescu,et al.  Erythrocyte structure and dynamics quantified by Hilbert phase microscopy. , 2005, Journal of biomedical optics.

[14]  B. Kemper,et al.  Digital holographic microscopy quantifies the degree of inflammation in experimental colitis. , 2013, Integrative biology : quantitative biosciences from nano to macro.

[15]  Aydogan Ozcan,et al.  Wide-field optical detection of nanoparticles using on-chip microscopy and self-assembled nanolenses , 2013, Nature Photonics.

[16]  E. Fort,et al.  Three-dimensional nanometre localization of nanoparticles to enhance super-resolution microscopy , 2015, Nature Communications.

[17]  Yibo Zhang,et al.  Phase recovery and holographic image reconstruction using deep learning in neural networks , 2017, Light: Science & Applications.

[18]  Jeeyeon Lee,et al.  Mitochondria-targeting indolizino[3,2-c]quinolines as novel class of photosensitizers for photodynamic anticancer activity. , 2018, European journal of medicinal chemistry.

[19]  B. Wattellier,et al.  Enhanced 3D spatial resolution in quantitative phase microscopy using spatially incoherent illumination. , 2014, Optics express.

[20]  E. Leith,et al.  Reconstructed Wavefronts and Communication Theory , 1962 .

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

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

[23]  K. Nugent,et al.  Noninterferometric phase imaging with partially coherent light , 1998 .

[24]  T. Poon Digital Holography and Three-Dimensional Display , 2006 .

[25]  Bertrand Simon,et al.  High‐resolution tomographic diffractive microscopy of biological samples , 2010, Journal of biophotonics.

[26]  Pasquale Memmolo,et al.  Tomographic flow cytometry by digital holography , 2016, Light: Science & Applications.

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

[28]  B. Wattellier,et al.  Quadriwave lateral shearing interferometry for quantitative phase microscopy of living cells. , 2009, Optics express.

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

[30]  V. Lauer New approach to optical diffraction tomography yielding a vector equation of diffraction tomography and a novel tomographic microscope , 2002, Journal of microscopy.

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

[32]  Milestones in light microscopy , 2009, Nature Cell Biology.

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

[34]  M. K. Kim,et al.  Tomographic three-dimensional imaging of a biological specimen using wavelength-scanning digital interference holography. , 2000, Optics express.

[35]  Aydogan Ozcan,et al.  Imaging without lenses: achievements and remaining challenges of wide-field on-chip microscopy , 2012, Nature Methods.

[36]  V. J. Francis Modern Electrical Engineering Mathematics , 1948, Nature.

[37]  Yibo Zhang,et al.  Extended depth-of-field in holographic image reconstruction using deep learning based auto-focusing and phase-recovery , 2018, Optica.

[38]  Pinhas Girshovitz,et al.  Interferometric phase microscopy for label-free morphological evaluation of sperm cells. , 2015, Fertility and sterility.

[39]  J. Rogers,et al.  Spatial light interference microscopy (SLIM) , 2010, IEEE Photonic Society 24th Annual Meeting.

[40]  R. Dasari,et al.  Diffraction phase microscopy for quantifying cell structure and dynamics. , 2006, Optics letters.

[41]  Yann Cotte,et al.  Realistic 3D coherent transfer function inverse filtering of complex fields , 2011, Biomedical optics express.

[42]  A. Michelson,et al.  On the relative motion of the Earth and the luminiferous ether , 1887, American Journal of Science.

[43]  Tan H. Nguyen,et al.  Gradient light interference microscopy for 3D imaging of unlabeled specimens , 2017, Nature Communications.

[44]  Joseph A Izatt,et al.  Spectral-domain phase microscopy. , 2004, Optics letters.

[45]  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.

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

[47]  Randy A Bartels,et al.  Single pixel quantitative phase imaging with spatial frequency projections. , 2017, Methods.

[48]  J. Tait,et al.  Challenges and opportunities. , 1996, Journal of psychiatric and mental health nursing.

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

[50]  Joseph M. Schmitt,et al.  Optical coherence tomography (OCT): a review , 1999 .

[51]  Zuowei Shen,et al.  Coherence Retrieval Using Trace Regularization , 2017, SIAM J. Imaging Sci..

[52]  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.

[53]  Gabriel Popescu,et al.  Label-Free Characterization of Emerging Human Neuronal Networks , 2014, Scientific Reports.

[54]  Yibo Zhang,et al.  Wide-field computational imaging of pathology slides using lens-free on-chip microscopy , 2014, Science Translational Medicine.

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

[56]  Taner Akkin,et al.  Spectral-domain optical coherence phase microscopy for quantitative phase-contrast imaging. , 2005, Optics letters.

[57]  Gabriel Popescu,et al.  Optical imaging of cell mass and growth dynamics. , 2008, American journal of physiology. Cell physiology.

[58]  F. Zernike How I discovered phase contrast. , 1955, Science.

[59]  M. Unser,et al.  Complex-wave retrieval from a single off-axis hologram. , 2004, Journal of the Optical Society of America. A, Optics, image science, and vision.

[60]  K. Nugent,et al.  Quantitative phase tomography , 2000 .

[61]  M. V. van Gemert,et al.  Two-dimensional birefringence imaging in biological tissue using polarization-sensitive optical coherence tomography , 1997, European Conference on Biomedical Optics.

[62]  Mbbs Md FRCPath Donald N. Pritzker Vinay Kumar Robbins and Cotran pathologic basis of disease , 2015 .

[63]  Reginald Birngruber,et al.  Optical coherence-gated imaging of biological tissues , 1996 .

[64]  Nicolas Pavillon,et al.  Noninvasive detection of macrophage activation with single-cell resolution through machine learning , 2018, Proceedings of the National Academy of Sciences.

[65]  Max Born,et al.  Principles of optics - electromagnetic theory of propagation, interference and diffraction of light (7. ed.) , 1999 .

[66]  M. Kirschner,et al.  Cell Growth and Size Homeostasis in Proliferating Animal Cells , 2009, Science.

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

[68]  V. Micó,et al.  Common-path phase-shifting digital holographic microscopy: A way to quantitative phase imaging and superresolution , 2008 .

[69]  Christian Depeursinge,et al.  Simultaneous Optical Recording in Multiple Cells by Digital Holographic Microscopy of Chloride Current Associated to Activation of the Ligand-Gated Chloride Channel GABAA Receptor , 2012, PloS one.

[70]  Zhuo Wang,et al.  Fourier transform light scattering of inhomogeneous and dynamic structures. , 2008, Physical review letters.

[71]  Frank Dubois,et al.  Partial spatial coherence effects in digital holographic microscopy with a laser source. , 2004, Applied optics.

[72]  Shuai Li,et al.  Lensless computational imaging through deep learning , 2017, ArXiv.

[73]  Shikhar Uttam,et al.  Early Prediction of Cancer Progression by Depth-Resolved Nanoscale Mapping of Nuclear Architecture from Unstained Tissue Specimens. , 2015, Cancer research.

[74]  E. Abbe Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung , 1873 .

[75]  A. Diaspro Optical Fluorescence Microscopy , 2011 .

[76]  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.

[77]  E. Wolf PHASE-MEASUREMENT INTERFEROMETRY TECHNIQUES , 2010 .

[78]  K. Creath V Phase-Measurement Interferometry Techniques , 1988 .

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

[80]  D Zicha,et al.  Dynamics of fibroblast spreading. , 1995, Journal of cell science.

[81]  S. Hell,et al.  Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. , 1994, Optics letters.

[82]  Jonghee Yoon,et al.  Holographic deep learning for rapid optical screening of anthrax spores , 2017, Science Advances.

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

[84]  YongKeun Park,et al.  Refractive index tomograms and dynamic membrane fluctuations of red blood cells from patients with diabetes mellitus , 2016, Scientific Reports.

[85]  R. C. Macridis A review , 1963 .

[86]  M S Feld,et al.  Interferometric phase-dispersion microscopy. , 2000, Optics letters.

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

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

[89]  Mark Bates,et al.  Super-resolution fluorescence microscopy. , 2009, Annual review of biochemistry.

[90]  E. Cuche,et al.  Digital holographic microscopy: a noninvasive contrast imaging technique allowing quantitative visualization of living cells with subwavelength axial accuracy. , 2005, Optics letters.

[91]  Simon Mitchell,et al.  Nongenetic origins of cell-to-cell variability in B lymphocyte proliferation , 2018, Proceedings of the National Academy of Sciences.

[92]  Nina Linder,et al.  Point-of-care mobile digital microscopy and deep learning for the detection of soil-transmitted helminths and Schistosoma haematobium , 2017, Global health action.

[93]  D. Gabor A New Microscopic Principle , 1948, Nature.

[94]  J. Mitchison,et al.  Growth during the cell cycle. , 2003, International review of cytology.

[95]  D. Sampson,et al.  Synthetic aperture fourier holographic optical microscopy. , 2006, Physical review letters.

[96]  Alberto Diaspro,et al.  Pushing phase and amplitude sensitivity limits in interferometric microscopy. , 2016, Optics letters.

[97]  A. Lohmann Optische Einseitenbandübertragung Angewandt auf das Gabor-Mikroskop , 1956 .

[98]  Ubin,et al.  Six-pack off-axis holography , 2017 .

[99]  Catherine Yourassowsky,et al.  High throughput holographic imaging-in-flow for the analysis of a wide plankton size range. , 2014, Optics express.

[100]  H. Bartelt,et al.  Image formation by inversion of scattered field data: experiments and computational simulation. , 1979, Applied optics.

[101]  J. Mitchison,et al.  Single cell studies of the cell cycle and some models , 2005, Theoretical Biology and Medical Modelling.

[102]  B. Berne,et al.  Dynamic Light Scattering: With Applications to Chemistry, Biology, and Physics , 1976 .

[103]  Daniel Carl,et al.  Investigation of living pancreas tumor cells by digital holographic microscopy. , 2006, Journal of biomedical optics.

[104]  M. Takeda,et al.  Fourier-transform method of fringe-pattern analysis for computer-based topography and interferometry , 1982 .

[105]  G. Truskey,et al.  Quantitative microscopy and nanoscopy of sickle red blood cells performed by wide field digital interferometry. , 2011, Journal of biomedical optics.

[106]  Chengshuai Li,et al.  Sensitivity evaluation of quantitative phase imaging: a study of wavelength shifting interferometry. , 2017, Optics letters.

[107]  J. Weitzman,et al.  Growing without a size checkpoint , 2003, Journal of biology.

[108]  Gabriel Popescu,et al.  Label-free quantitative evaluation of breast tissue using Spatial Light Interference Microscopy (SLIM) , 2018, Scientific Reports.

[109]  Barry R. Masters,et al.  Quantitative Phase Imaging of Cells and Tissues , 2012 .

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

[111]  Young Jae Lee,et al.  Magnified Image Spatial Spectrum (MISS) microscopy for nanometer and millisecond scale label-free imaging. , 2018, Optics express.

[112]  YongKeun Park,et al.  Identification of non-activated lymphocytes using three-dimensional refractive index tomography and machine learning , 2017, Scientific Reports.

[113]  Miroslav Hejna,et al.  High accuracy label-free classification of single-cell kinetic states from holographic cytometry of human melanoma cells , 2017, Scientific Reports.

[114]  Myung K. Kim,et al.  Measurement of the traction force of biological cells by digital holography , 2011, Biomedical optics express.

[115]  Gabriel Popescu,et al.  Tissue refractometry using Hilbert phase microscopy. , 2007, Optics letters.

[116]  Manuel Bedrossian,et al.  Digital Holographic Microscopy, a Method for Detection of Microorganisms in Plume Samples from Enceladus and Other Icy Worlds , 2017, Astrobiology.

[117]  P. Barber Absorption and scattering of light by small particles , 1984 .

[118]  J. Izatt,et al.  In vivo bidirectional color Doppler flow imaging of picoliter blood volumes using optical coherence tomography. , 1997, Optics letters.

[119]  M. Langlois,et al.  Society of Photo-Optical Instrumentation Engineers , 2005 .

[120]  Radim Chmelík,et al.  Coherence-controlled holographic microscope. , 2010, Optics express.

[121]  Zhuo Wang,et al.  Dispersion-relation phase spectroscopy of intracellular transport , 2011, Optics express.

[122]  M S Feld,et al.  Phase-referenced interferometer with subwavelength and subhertz sensitivity applied to the study of cell membrane dynamics. , 2001, Optics letters.

[123]  H. G. Davies,et al.  Interference Microscopy and Mass Determination , 1952, Nature.

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

[125]  A. Stoica,et al.  The adhesion of normal human dermal fibroblasts to the cyclopropylamine plasma polymers studied by holographic microscopy , 2016 .

[126]  Graham Dunn,et al.  An image processing system for cell behaviour studies in subconfluent cultures , 1995 .

[127]  Steffi Ketelhut,et al.  Quantitative Stain-Free and Continuous Multimodal Monitoring of Wound Healing In Vitro with Digital Holographic Microscopy , 2014, PloS one.