Bioimpedance Spectroscopy: Basics and Applications.

In this review, we aim to introduce the reader to the technique of electrical impedance spectroscopy (EIS) with a focus on its biological and medical applications. We explain the theoretical and experimental aspects of the EIS with the details essential for biological studies, i.e interaction of metal electrodes with biological matter and liquids, strategies of increasing measurement rate and noise reduction in bio-EIS experiments, etc. We give various examples of successful bio-EIS practical implementations in science and technology: from the whole-body health monitoring and sensors for vision prosthetic care to single living cell examination platforms and virus diseases research. Present review can be used as a bio-EIS tutorial for students as well as a handbook for scientists and engineers due to extensive references covering the contemporary research papers in the field.

[1]  Su-Moon Park,et al.  Electrochemical impedance spectroscopy. , 2010, Annual review of analytical chemistry.

[2]  J. Luther,et al.  Predictive Mechanistic Model for the Electrical Impedance and Intensity-Modulated Photocurrent and Photovoltage Spectroscopic Responses of an Organic Bulk Heterojunction Solar Cell , 2016 .

[3]  G. Reinsel,et al.  Introduction to Mathematical Statistics (4th ed.). , 1980 .

[4]  Zhenyu Guo,et al.  A review of electrical impedance techniques for breast cancer detection. , 2003, Medical engineering & physics.

[5]  Jian Xu,et al.  Single-cell bioelectrical impedance platform for monitoring cellular response to drug treatment , 2011, Physical biology.

[6]  Yu-Te Liao,et al.  A 3-$\mu\hbox{W}$ CMOS Glucose Sensor for Wireless Contact-Lens Tear Glucose Monitoring , 2012, IEEE Journal of Solid-State Circuits.

[7]  Vadim F. Lvovich,et al.  Impedance Spectroscopy: Applications to Electrochemical and Dielectric Phenomena , 2012 .

[8]  D. Mondal,et al.  Extended Electrical Model for Impedance Characterization of Cultured HeLa Cells in Non-Confluent State Using ECIS Electrodes , 2013, IEEE Transactions on NanoBioscience.

[9]  Marion C Lanteri,et al.  Serum from dengue virus-infected patients with and without plasma leakage differentially affects endothelial cells barrier function in vitro , 2017, PloS one.

[10]  J. Ross Macdonald,et al.  Applicability and power of complex nonlinear least squares for the analysis of impedance and admittance data , 1982 .

[11]  A. Marghoob,et al.  Electrical Impedance Spectroscopy in Skin Cancer Diagnosis. , 2017, Dermatologic clinics.

[12]  K. Cole.  ELECTRIC IMPEDANCE OF SUSPENSIONS OF ARBACIA EGGS , 1928, The Journal of general physiology.

[13]  G. Barbero,et al.  Evidence of the ambipolar diffusion in the impedance spectroscopy of an electrolytic cell. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[14]  A. Malik,et al.  Electrical method for detection of endothelial cell shape change in real time: assessment of endothelial barrier function. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[15]  M. Thompson,et al.  Probing the bioelectrochemistry of living cells , 2008 .

[16]  Yi-Tao Long,et al.  AC impedance spectroscopy of native DNA and M-DNA. , 2003, Biophysical journal.

[17]  Brian H. Brown,et al.  Medical impedance tomography and process impedance tomography: a brief review , 2001 .

[18]  Digby D. Macdonald,et al.  A Method for Estimating Impedance Parameters for Electrochemical Systems That Exhibit Pseudoinductance , 1978 .

[19]  John H T Luong,et al.  On‐Line Monitoring of Cell Growth and Cytotoxicity Using Electric Cell‐Substrate Impedance Sensing (ECIS) , 2003, Biotechnology progress.

[20]  Ping Wang,et al.  Cell-based biosensors : principles and applications , 2010 .

[21]  T. Dzieciątkowski,et al.  The xCELLigence system for real-time and label-free analysis of neuronal and dermal cell response to equine herpesvirus type 1 infection. , 2012, Polish journal of veterinary sciences.

[22]  D. D. Stupin,et al.  Cell-Substrate Lift-off Lithography: Proof of Concept , 2018, Journal of Physics: Conference Series.

[23]  P. Delahay,et al.  Double Layer and Electrode Kinetics , 1965 .

[24]  Ivar Giaever,et al.  A morphological biosensor for mammalian cells , 1993, Nature.

[25]  Ananth Ranganathan,et al.  The Levenberg-Marquardt Algorithm , 2004 .

[26]  Keith D. Paulsen,et al.  Electrical impedance spectroscopy of the breast: clinical imaging results in 26 subjects , 2002, IEEE Transactions on Medical Imaging.

[27]  Jeffrey C. Lagarias,et al.  Convergence Properties of the Nelder-Mead Simplex Method in Low Dimensions , 1998, SIAM J. Optim..

[28]  H. Bank.  Rapid assessment of islet viability with acridine orange and propidium iodide , 1988, In Vitro Cellular & Developmental Biology.

[29]  Shaojun Dong,et al.  Kinetic study of DNA/DNA hybridization with electrochemical impedance spectroscopy , 2007 .

[30]  T. M. Brown,et al.  By Electrochemical methods , 2007 .

[31]  J. Wegener,et al.  Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces. , 2000, Experimental cell research.

[32]  Ulrich Tietze,et al.  Electronic Circuits: Handbook for Design and Application , 1991 .

[33]  Sungbo Cho,et al.  Impedance monitoring of herpes simplex virus-induced cytopathic effect in Vero cells , 2007 .

[34]  R. Kant,et al.  Debye–Falkenhagen dynamics of electric double layer in presence of electrode heterogeneities , 2013 .

[35]  Yvonne Hsu-Lin Luo,et al.  MRI brain scans in two patients with the argus II retinal prosthesis. , 2013, Ophthalmology.

[36]  Miqin Zhang,et al.  Cellular impedance biosensors for drug screening and toxin detection. , 2007, The Analyst.

[37]  D. Franceschetti,et al.  Theory of small‐signal ac response of solids and liquids with recombining mobile charge , 1978 .

[38]  Z. Teng,et al.  Real-time cell analysis--a new method for dynamic, quantitative measurement of infectious viruses and antiserum neutralizing activity. , 2013, Journal of virological methods.

[39]  Michio Niwano,et al.  Dependence and Homeostasis of Membrane Impedance on Cell Morphology in Cultured Hippocampal Neurons , 2018, Scientific Reports.

[40]  Soumen Das,et al.  Quantitative evaluation of blood glucose concentration using impedance sensing devices , 2013 .

[41]  Chun-Min Lo,et al.  A Detailed Model for High-Frequency Impedance Characterization of Ovarian Cancer Epithelial Cell Layer Using ECIS Electrodes , 2009, IEEE Transactions on Biomedical Engineering.

[42]  E. Król,et al.  Universal biosensor for detection of influenza virus. , 2014, Biosensors & bioelectronics.

[43]  Karsten Nielsen,et al.  The Active Pulse Modulated Transducer (AT) - A Novel Audio Power Conversion System Architecture , 2003 .

[44]  David C. Martin,et al.  Polymerization of the conducting polymer poly(3,4-ethylenedioxythiophene) (PEDOT) around living neural cells. , 2007, Biomaterials.

[45]  R. Harikumar,et al.  Electrical Impedance Tomography (EIT) and Its Medical Applications: A Review , 2013 .

[46]  O. Kanoun.  Impedance Spectroscopy : Advanced Applications: Battery Research, Bioimpedance, System Design , 2019 .

[47]  R. D. Levie,et al.  The influence of surface roughness of solid electrodes on electrochemical measurements , 1965 .

[48]  W. Jiang,et al.  Electric Cell-Substrate Impedance Sensing and Cancer Metastasis , 2012, Cancer Metastasis - Biology and Treatment.

[49]  Josep Samitier,et al.  A novel detection strategy for odorant molecules based on controlled bioengineering of rat olfactory receptor I7. , 2007, Biosensors & bioelectronics.

[50]  J. A. Garber,et al.  Analysis of Impedance and Admittance Data for Solids and Liquids , 1977 .

[51]  D. Macdonald.  Reflections on the history of electrochemical impedance spectroscopy , 2006 .

[52]  Xiao Xu,et al.  The xCELLigence system for real-time and label-free monitoring of cell viability. , 2011, Methods in molecular biology.

[53]  H. Itoh,et al.  Time courses of cell electroporation as revealed by submicrosecond imaging of transmembrane potential. , 1993, Biophysical journal.

[54]  B. Hu.  Kramers-Kronig in two lines , 1989 .

[55]  B. Widrow,et al.  Adaptive noise cancelling: Principles and applications , 1975 .

[56]  Andreas Hierlemann,et al.  Impedance characterization and modeling of electrodes for biomedical applications , 2005, IEEE Transactions on Biomedical Engineering.

[57]  H. Curtis,et al.  TRANSVERSE ELECTRIC IMPEDANCE OF NITELLA , 1937, The Journal of general physiology.

[58]  DAVID G. KENDALL,et al.  Introduction to Mathematical Statistics , 1947, Nature.

[59]  Ivar Giaever,et al.  Monitoring viral-induced cell death using electric cell-substrate impedance sensing. , 2007, Biosensors & bioelectronics.

[60]  N. Jaffrezic‐Renault,et al.  Miniaturized biosensor for avian influenza virus detection , 2008 .

[61]  T. Pajkossy,et al.  On the origin of capacitance dispersion of rough electrodes , 2000 .

[62]  J. Masters.  HeLa cells 50 years on: the good, the bad and the ugly , 2002, Nature Reviews Cancer.

[63]  T. Pajkossy,et al.  Impedance of rough capacitive electrodes , 1994 .

[64]  Meisam Tabatabaei,et al.  A review on emerging diagnostic assay for viral detection: the case of avian influenza virus , 2014, Molecular Biology Reports.

[65]  D. D. Stupin,et al.  TiN Nanoporous Electrode Covered by Single Cell as Bio-Electronic Sensor of Radiation Hazard , 2018 .

[66]  R. Rabbitt,et al.  A Multilayer MEMS Platform for Single-Cell Electric Impedance Spectroscopy and Electrochemical Analysis , 2008, Journal of Microelectromechanical Systems.

[67]  Joachim Wegener,et al.  Electrical wound-healing assay for cells in vitro. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[68]  D. D. Stupin.  The Single Cells and Cell Populations Viability Estimation in vitro by the Time-Domain Impedance Spectroscopy , 2018, Technical Physics.

[69]  R. N. Schindler,et al.  A new impedance spectrometer for the investigation of electrochemical systems , 1992 .

[70]  Michael J van Rijssel,et al.  Comparison of cardiac time intervals between echocardiography and impedance cardiography at various heart rates , 2014 .

[71]  S. Sekaran,et al.  Japanese encephalitis virus disrupts blood-brain barrier and modulates apoptosis proteins in THBMEC cells. , 2017, Virus Research.

[72]  D. D. Stupin.  A Single-Cell Electronic Sensor of Toxins , 2017 .

[73]  Leon S. Oleg Theremin,et al.  The Design of a Musical Instrument Based on Cathode Relays , 1996 .

[74]  E. C. Levy.  Complex-curve fitting , 1959, IRE Transactions on Automatic Control.

[75]  H. L,et al.  Electrical Papers , 1893, Nature.

[76]  K. Cole.  ELECTRIC IMPEDANCE OF SUSPENSIONS OF SPHERES , 1928, The Journal of general physiology.

[77]  K. Mølhave,et al.  Mapping the Complex Morphology of Cell Interactions with Nanowire Substrates Using FIB-SEM , 2013, PloS one.

[78]  Gerhard Hummer,et al.  Ion sizes and finite-size corrections for ionic-solvation free energies , 1997 .

[79]  A. N. Nordin,et al.  Electrical cell-substrate impedance sensing (ECIS) based biosensor for characterization of DF-1 cells , 2010, International Conference on Computer and Communication Engineering (ICCCE'10).

[80]  W. Hassen,et al.  Quantitation of influenza A virus in the presence of extraneous protein using electrochemical impedance spectroscopy , 2011 .

[81]  Xingqun Jiang,et al.  Electrochemical impedance biosensor with electrode pixels for precise counting of CD4+ cells: a microchip for quantitative diagnosis of HIV infection status of AIDS patients. , 2010, Biosensors & bioelectronics.

[82]  M. Verbrugge,et al.  Battery State Estimator Based on a Finite Impulse Response Filter , 2013 .

[83]  Lei Wang,et al.  Analysis of the sensitivity and frequency characteristics of coplanar electrical cell-substrate impedance sensors. , 2008, Biosensors & bioelectronics.

[84]  V. V. Brus,et al.  On impedance spectroscopy analysis of nonideal heterojunctions , 2012 .

[85]  Ayae Honda,et al.  Nonlinear electrical impedance spectroscopy of viruses using very high electric fields created by nanogap electrodes , 2015, Front. Microbiol..

[86]  G. R. Van de Walle,et al.  Electric Cell-Substrate Impedance Sensing To Monitor Viral Growth and Study Cellular Responses to Infection with Alphaherpesviruses in Real Time , 2017, mSphere.

[87]  L. Reggiani,et al.  Role of topology in electrical properties of bacterio-rhodopsin and rat olfactory receptor I7. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[88]  H. Bogaard,et al.  Electric Cell-substrate Impedance Sensing for the Quantification of Endothelial Proliferation, Barrier Function, and Motility , 2014, Journal of visualized experiments : JoVE.

[89]  Junhong Min,et al.  Electric Cell-Substrate Impedance Sensing (ECIS) with Microelectrode Arrays for Investigation of Cancer Cell – Fibroblasts Interaction , 2016, PloS one.

[90]  Liu.  Fractal model for the ac response of a rough interface. , 1985, Physical review letters.

[91]  Clay W Scott,et al.  Human Stem Cell-Derived Cardiomyocytes in Cellular Impedance Assays: Bringing Cardiotoxicity Screening to the Front Line , 2014, Cardiovascular Toxicology.

[92]  Andrzej Lasia,et al.  Influence of experimental factors on the constant phase element behavior of Pt electrodes , 2011 .

[94]  R. Kant,et al.  Theory of anomalous dynamics of electric double layer at heterogeneous and rough electrodes , 2014 .

[95]  D. D. Stupin,et al.  Adaptive Filtering to Enhance Noise Immunity of Impedance and Admittance Spectroscopy: Comparison with Fourier Transformation , 2017, 1701.06503.

[96]  Robert Plonsey,et al.  Bioelectricity: A Quantitative Approach Duke University’s First MOOC , 2013 .

[97]  Katja Lindenberg,et al.  Extinction in population dynamics. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[98]  H. Föll,et al.  FFT impedance spectroscopy analysis of the growth of anodic oxides on (100) p-Si for various solvents , 2008 .

[99]  Hanry Yu,et al.  Label‐free virus identification and characterization using electrochemical impedance spectroscopy , 2014, Electrophoresis.

[100]  Giovanni Barbero,et al.  Effect of different anionic and cationic mobilities on the impedance spectroscopy measurements , 2005 .

[101]  Karine Reybier,et al.  Fibroblast cells: a sensing bioelement for glucose detection by impedance spectroscopy. , 2003, Analytical chemistry.

[102]  E. Barsoukov,et al.  Impedance spectroscopy : theory, experiment, and applications , 2005 .

[103]  G. Ferrari,et al.  Capacitance Spectroscopy of Semiconductors , 2018 .

[104]  Eugenia Wang,et al.  Use of electric cell-substrate impedance sensing as a tool for quantifying cytopathic effect in influenza A virus infected MDCK cells in real-time. , 2005, Journal of virological methods.

[105]  F. Golnaraghi,et al.  Cancer Detection Based on Electrical Impedance Spectroscopy: A Clinical Study , 2018, Journal of electrical bioimpedance.

[106]  R H Bayford,et al.  Bioimpedance tomography (electrical impedance tomography). , 2006, Annual review of biomedical engineering.

[107]  Y. Tsai,et al.  Nonlinear least-squares analyses of complex impedance and admittance data for solid electrolytes , 1982 .