Optical spectroscopy and imaging for the noninvasive evaluation of engineered tissues.

Optical spectroscopy and imaging approaches offer the potential to noninvasively assess different aspects of the cellular, extracellular matrix, and scaffold components of engineered tissues. In addition, the combination of multiple imaging modalities within a single instrument is highly feasible, allowing acquisition of complementary information related to the structure, organization, biochemistry, and physiology of the sample. The ability to characterize and monitor the dynamic interactions that take place as engineered tissues develop promises to enhance our understanding of the interdependence of processes that ultimately leads to functional tissue outcomes. It is expected that this information will impact significantly upon our abilities to optimize the design of biomaterial scaffolds, bioreactors, and cell systems. Here, we review the principles and performance characteristics of the main methodologies that have been exploited thus far, and we present examples of corresponding tissue engineering studies.

[1]  Barry Cense,et al.  Advances in optical coherence tomography imaging for dermatology. , 2004, The Journal of investigative dermatology.

[2]  E. Sevick-Muraca,et al.  Quantitative optical spectroscopy for tissue diagnosis. , 1996, Annual review of physical chemistry.

[3]  Bruce J Tromberg,et al.  Imaging coronary artery microstructure using second-harmonic and two-photon fluorescence microscopy. , 2004, Biophysical journal.

[4]  Seeram Ramakrishna,et al.  Electrospun nanofiber fabrication as synthetic extracellular matrix and its potential for vascular tissue engineering. , 2004, Tissue engineering.

[5]  Ruikang K. Wang,et al.  Investigation of optical coherence tomography as an imaging modality in tissue engineering , 2006, Physics in medicine and biology.

[6]  J. Paul Robinson,et al.  Analysis of Orientations of Collagen Fibers by Novel Fiber-Tracking Software , 2003, Microscopy and Microanalysis.

[7]  N. Turner,et al.  A novel hyaluronan-based biomaterial (Hyaff-11) as a scaffold for endothelial cells in tissue engineered vascular grafts. , 2004, Biomaterials.

[8]  M. Först,et al.  High‐resolution optical coherence tomography as a non‐destructive monitoring tool for the engineering of skin equivalents , 2006, Skin research and technology : official journal of International Society for Bioengineering and the Skin (ISBS) [and] International Society for Digital Imaging of Skin (ISDIS) [and] International Society for Skin Imaging.

[9]  F. A. Navarro,et al.  Two-Photon Confocal Microscopy: A Nondestructive Method for Studying Wound Healing , 2004, Plastic and reconstructive surgery.

[10]  Tejal A Desai,et al.  Optical coherence tomography of cell dynamics in three-dimensional tissue models. , 2006, Optics express.

[11]  William A Mohler,et al.  Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues. , 2002, Biophysical journal.

[12]  Kam W Leong,et al.  Adhesion contact dynamics of primary hepatocytes on poly(ethylene terephthalate) surface. , 2004, Biomaterials.

[13]  P Dunnill,et al.  Doppler optical coherence tomography for measuring flow in engineered tissue. , 2004, Biosensors & bioelectronics.

[14]  Irene Georgakoudi,et al.  Non-invasive optical characterization of biomaterial mineralization. , 2008, Biomaterials.

[15]  Joseph J Pancrazio,et al.  Enabling tools for tissue engineering. , 2007, Biosensors & bioelectronics.

[16]  J. Pawley,et al.  Handbook of Biological Confocal Microscopy , 1990, Springer US.

[17]  D. Leckband,et al.  Structural and functional optical imaging of three-dimensional engineered tissue development. , 2004, Tissue engineering.

[18]  William A Mohler,et al.  Coherent and incoherent SHG in fibrillar cellulose matrices. , 2007, Optics express.

[19]  I Gryczynski,et al.  Fluorescence of reduced nicotinamides using one- and two-photon excitation. , 1996, Biophysical chemistry.

[20]  Jens Eickhoff,et al.  In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia. , 2007, Journal of biomedical optics.

[21]  K. Fujita.  [Two-photon laser scanning fluorescence microscopy]. , 2007, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[22]  Michael S. Feld,et al.  Measuring cellular structure at submicrometer scale with light scattering spectroscopy , 2001 .

[23]  S. Boppart,et al.  Optical coherence elastography of engineered and developing tissue. , 2006, Tissue engineering.

[24]  Kristi S Anseth,et al.  Three-dimensional growth and function of neural tissue in degradable polyethylene glycol hydrogels. , 2006, Biomaterials.

[25]  M Rajadhyaksha,et al.  Topographic variations in normal skin, as viewed by in vivo reflectance confocal microscopy. , 2001, The Journal of investigative dermatology.

[26]  Katja Schenke-Layland,et al.  Tissue engineering of aortic tissue: dire consequence of suboptimal elastic fiber synthesis in vivo. , 2004, Cardiovascular research.

[27]  Tasshi Dennis,et al.  Phase-dispersion light scattering for quantitative size-imaging of spherical scatterers , 2007, SPIE BiOS.

[28]  OrenCaspi,et al.  Tissue Engineering of Vascularized Cardiac Muscle From Human Embryonic Stem Cells , 2007 .

[29]  Joshua Pfefer,et al.  Depth-sensitive reflectance measurements using obliquely oriented fiber probes. , 2005, Journal of biomedical optics.

[30]  Watt W Webb,et al.  Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein. , 2002, Biophysical journal.

[31]  Claudio Vinegoni,et al.  Spectroscopic spectral-domain optical coherence microscopy. , 2006, Optics letters.

[32]  W Matthew Petroll,et al.  Quantitative assessment of local collagen matrix remodeling in 3-D culture: the role of Rho kinase. , 2006, Experimental cell research.

[33]  Suresh Valiyaveettil,et al.  Developing macroporous bicontinuous materials as scaffolds for tissue engineering. , 2005, Biomaterials.

[34]  I Gryczynski,et al.  Fluorescence anisotropy of tyrosine using one-and two-photon excitation. , 1995, Biophysical chemistry.

[35]  Salvador González,et al.  In vivo reflectance‐mode confocal microscopy in clinical dermatology and cosmetology , 2008, International journal of cosmetic science.

[36]  Chen-Yuan Dong,et al.  Imaging human bone marrow stem cell morphogenesis in polyglycolic acid scaffold by multiphoton microscopy. , 2006, Tissue engineering.

[37]  B. Bouma,et al.  Improved signal-to-noise ratio in spectral-domain compared with time-domain optical coherence tomography. , 2003, Optics letters.

[38]  Andreas Zumbusch,et al.  Coherent anti-Stokes Raman scattering microscopy , 1999 .

[39]  R K Wang,et al.  The potential of optical coherence tomography in the engineering of living tissue. , 2004, Physics in medicine and biology.

[40]  Watt W. Webb,et al.  Multiphoton excitation cross‐sections of molecular fluorophores , 1996 .

[41]  Bruce J Tromberg,et al.  Imaging wound healing using optical coherence tomography and multiphoton microscopy in an in vitro skin-equivalent tissue model. , 2004, Journal of biomedical optics.

[42]  Salman Rosenwaks,et al.  Probing the effect of an extract of elk velvet antler powder on mesenchymal stem cells using Raman microspectroscopy: enhanced differentiation toward osteogenic fate , 2006 .

[43]  Vadim Backman,et al.  Simultaneous measurement of angular and spectral properties of light scattering for characterization of tissue microarchitecture and its alteration in early precancer , 2003 .

[44]  W. Webb,et al.  Water-Soluble Quantum Dots for Multiphoton Fluorescence Imaging in Vivo , 2003, Science.

[45]  Dietmar W. Hutmacher,et al.  Characterization of Osteogenically Induced Adipose Tissue-Derived Precursor Cells in 2-Dimensional and 3-Dimensional Environments , 2006, Cells Tissues Organs.

[46]  Y. Yang,et al.  Chitosan microchannel scaffolds for tendon tissue engineering characterized using optical coherence tomography. , 2007, Tissue engineering.

[47]  K. König,et al.  Multiphoton autofluorescence imaging of intratissue elastic fibers. , 2005, Biomaterials.

[48]  Vincent Chan,et al.  Adhesion contact dynamics of fibroblasts on biomacromolecular surfaces. , 2005, Macromolecular bioscience.

[49]  W. Denk,et al.  Two-photon imaging to a depth of 1000 microm in living brains by use of a Ti:Al2O3 regenerative amplifier. , 2003, Optics letters.

[50]  Oksana Kostyuk,et al.  Novel spectroscopic technique for in situ monitoring of collagen fibril alignment in gels. , 2004, Biophysical journal.

[51]  Laura Marcu,et al.  Noninvasive in situ evaluation of osteogenic differentiation by time-resolved laser-induced fluorescence spectroscopy. , 2004, Tissue engineering.

[52]  Veerle Cnudde,et al.  Porous gelatin hydrogels: 2. In vitro cell interaction study. , 2007, Biomacromolecules.

[53]  G. Patterson,et al.  Photobleaching in two-photon excitation microscopy. , 2000, Biophysical journal.

[54]  W. Webb,et al.  Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[55]  David L. Kaplan,et al.  Quantitative biomarkers of stem cell differentiation based on intrinsic two-photon excited fluorescence. , 2007, Journal of biomedical optics.

[56]  Young L. Kim,et al.  Endogenous optical biomarkers of normal and human papillomavirus immortalized epithelial cells , 2008, International journal of cancer.

[57]  Qingling Feng,et al.  Materials Selection and Scaffold Construction for Liver Tissue Engineering , 2005 .

[58]  Ruikang K. Wang,et al.  Investigation of changes in optical attenuation of bone and neuronal cells in organ culture or three-dimensional constructs in vitro with optical coherence tomography: relevance to cytochrome oxidase monitoring , 2003, European Biophysics Journal.

[59]  Karsten König,et al.  Imaging of cardiovascular structures using near-infrared femtosecond multiphoton laser scanning microscopy. , 2005, Journal of biomedical optics.

[60]  Jean François Stoltz,et al.  Optimisation of Biochemical Condition and Substrates In Vitro for Tissue Engineering of Ligament , 2006, Annals of Biomedical Engineering.

[61]  Irene Georgakoudi,et al.  Non-invasive characterization of structure and morphology of silk fibroin biomaterials using non-linear microscopy. , 2008, Biomaterials.

[62]  Ung-Jin Kim,et al.  In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells. , 2005, Biomaterials.

[63]  Frederick Grinnell,et al.  Modulation of fibroblast morphology and adhesion during collagen matrix remodeling. , 2002, Molecular biology of the cell.

[64]  K. Badizadegan,et al.  Fluorescence, reflectance, and light-scattering spectroscopy for evaluating dysplasia in patients with Barrett's esophagus. , 2001, Gastroenterology.

[65]  Antonios G Mikos,et al.  Effect of flow perfusion on the osteogenic differentiation of bone marrow stromal cells cultured on starch-based three-dimensional scaffolds. , 2003, Journal of biomedical materials research. Part A.

[66]  Constantinos Pitris,et al.  Optical imaging of the cervix , 2003, Cancer.

[67]  I. Titushkin,et al.  Regulation of mesenchymal stem cell adhesion and orientation in 3D collagen scaffold by electrical stimulus. , 2006, Bioelectrochemistry.

[68]  K. Augsten,et al.  Handbook of Biological Confocal Microscopy. : J.B. Pawley (Editor), Plenum Press, New York, 1990, xiii + 232 pp., ISBN 0-306-43538-1. , 1992 .

[69]  Oksana Kostyuk,et al.  Structural changes in loaded equine tendons can be monitored by a novel spectroscopic technique , 2004, The Journal of physiology.

[70]  K. König,et al.  Two-photon microscopes and in vivo multiphoton tomographs--powerful diagnostic tools for tissue engineering and drug delivery. , 2006, Advanced drug delivery reviews.

[71]  Alfons Penzkofer,et al.  Photo-induced degradation of some flavins in aqueous solution , 2005 .

[72]  Sheng Lin-Gibson,et al.  Tissue engineering scaffolds based on photocured dimethacrylate polymers for in vitro optical imaging. , 2006, Biomacromolecules.

[73]  T. G. Scott,et al.  Synthetic spectroscopic models related to coenzymes and base pairs. V. Emission properties of NADH. Studies of fluorescence lifetimes and quantum efficiencies of NADH, AcPyADH, [reduced acetylpyridineadenine dinucleotide] and simplified synthetic models , 1970 .

[74]  Salvador Gonzalez,et al.  Tissue Engineered Cartilage Integration to Live and Devitalized Cartilage: A Study by Reflectance Mode Confocal Microscopy and Standard Histology , 2006, Connective tissue research.

[75]  U. Cogan,et al.  Binding affinities of retinol and related compounds to retinol binding proteins. , 1976, European journal of biochemistry.

[76]  B. Tromberg,et al.  Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Michele Follen,et al.  Spatially resolved reflectance spectroscopy for diagnosis of cervical precancer: Monte Carlo modeling and comparison to clinical measurements. , 2006, Journal of biomedical optics.

[78]  Judith M Curran,et al.  The differentiation of bone marrow mesenchymal stem cells into chondrocyte-like cells on poly-L-lactic acid (PLLA) scaffolds. , 2006, Biomaterials.

[79]  U Kneser,et al.  Modulation of in vitro angiogenesis in a three-dimensional spheroidal coculture model for bone tissue engineering. , 2004, Tissue engineering.

[80]  Sun Ig Hong,et al.  Spatial control of protein within biomimetically nucleated mineral. , 2006, Biomaterials.

[81]  Yun-shan Zhao,et al.  Construction of a unidirectionally beating 3-dimensional cardiac muscle construct. , 2005, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[82]  Hans C Gerritsen,et al.  Spectrally resolved multiphoton imaging of in vivo and excised mouse skin tissues. , 2007, Biophysical journal.

[83]  A. Tsai,et al.  Redox Properties of Human Endothelial Nitric-oxide Synthase Oxygenase and Reductase Domains Purified from Yeast Expression System* , 2003, The Journal of Biological Chemistry.

[84]  J F Stoltz,et al.  Spectral and lifetime fluorescence imaging microscopies: new modalities of multiphoton microscopy applied to tissue or cell engineering. , 2004, Biorheology.

[85]  J. Squirrell,et al.  Imaging Mitochondrial Organization in Living Primate Oocytes and Embryos using Multiphoton Microscopy , 2003, Microscopy and Microanalysis.

[86]  Irene Georgakoudi,et al.  Intrinsic fluorescence changes associated with the conformational state of silk fibroin in biomaterial matrices. , 2007, Optics express.

[87]  F. I. Hárosi,et al.  Solubility of retinoids in water. , 1991, Archives of biochemistry and biophysics.

[88]  Meng-Tsan Tsai,et al.  Measurement of the hemoglobin oxygen saturation level with spectroscopic spectral-domain optical coherence tomography. , 2008, Optics letters.

[89]  Swee Hin Teoh,et al.  Nanofibrous modification on ultra-thin poly(e-caprolactone) membrane via electrospinning , 2007 .

[90]  F. Ren,et al.  Confocal laser scanning microscopy as a tool for imaging cancellous bone. , 2006, Journal of biomedical materials research. Part B, Applied biomaterials.

[91]  W Matthew Petroll,et al.  Differential interference contrast and confocal reflectance imaging of collagen organization in three-dimensional matrices. , 2007, Scanning.

[92]  Ioan Notingher,et al.  In situ spectral monitoring of mRNA translation in embryonic stem cells during differentiation in vitro. , 2004, Analytical chemistry.

[93]  P. B. Cipolloni,et al.  Noninvasive sizing of subcellular organelles with light scattering spectroscopy , 2003 .

[94]  Yang Liu,et al.  Spectroscopic translation of cell-material interactions. , 2007, Biomaterials.

[95]  S. Jacques,et al.  Light Distributions from Point, Line and Plane Sources for Photochemical Reactions and Fluorescence in Turbid Biological Tissues , 1998, Photochemistry and photobiology.

[96]  Irene Georgakoudi,et al.  Trimodal spectroscopy for the detection and characterization of cervical precancers in vivo. , 2002, American journal of obstetrics and gynecology.