Cellular electrical impedance spectroscopy: An emerging technology of microscale biosensors

Expert Review of Medical Devices

Volumn 7, Issue 6, 2010, Pages 767-779

  Gu, Wenwen ^a,b   Zhao, Yi ^b  

^a CHONGQING UNIVERSITY   (China)

^b Ohio State University   (United States)

Author keywords

cell migration; cytotoxicity; electric cell substrate impedance spectroscopy; impedance spectroscopy; ion release; lab on chip; microfluidics; microsensors

Indexed keywords

CELL MIGRATION; ELECTRIC CELLS; IMPEDANCE SPECTROSCOPY; ION RELEASE; LAB-ON-CHIP;

BIOSENSORS; CYTOTOXICITY; DRUG THERAPY; ELECTRIC IMPEDANCE MEASUREMENT; IONS; MICROFLUIDICS; MICROSENSORS; RHEOLOGY;

ELECTRIC IMPEDANCE;

CISPLATIN; GOLD NANOPARTICLE; QUANTUM DOT;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BIOSENSOR; BLOOD FLOW VELOCITY; BLOOD RHEOLOGY; CELL ADHESION; CELL GROWTH; CELL MEMBRANE CONDUCTANCE; CELL MOTILITY; CELL SPREADING; CELL SUSPENSION; CELLULAR DISTRIBUTION; CLINICAL EFFECTIVENESS; COST EFFECTIVENESS ANALYSIS; CYTOLOGY; DRUG CYTOTOXICITY; DRUG RESEARCH; ELECTRIC FIELD; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; EQUIPMENT DESIGN; HUMAN; INTERMETHOD COMPARISON; ION TRANSPORT; LAB ON A CHIP; MICROELECTRODE; MICROTECHNOLOGY; NANOTECHNOLOGY; NONHUMAN; PHYSICAL MODEL; PROCESS DEVELOPMENT; PROCESS MODEL; REVIEW; SENSITIVITY AND SPECIFICITY; STRUCTURE ANALYSIS; WOUND HEALING;

BIOSENSING TECHNIQUES; BIOTECHNOLOGY; CELL PHYSIOLOGICAL PHENOMENA; DIELECTRIC SPECTROSCOPY; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; MINIATURIZATION;

EID: 78149421243     PISSN: 17434440     EISSN: 17452422     Source Type: Journal    
DOI: 10.1586/erd.10.47     Document Type: Review

References (102)

1. Torrents JM, Juan-Garcia P, Aguado A. Electrical impedance spectroscopy as a technique for the surveillance of civil engineering structures: considerations on the galvanic insulation of samples. Meas. Sci. Technol. 18, 1958-1962 (2007).
2. Wu J, Ben Y, Chang HC. Particle detection by electrical impedance spectroscopy with asymmetric-polarization AC electroosmotic trapping. Microfluid. Nanofluid. 1, 161-167 (2005).
3. Casas O, Bragos R, Riu PJ et al. In vivo and in situ ischemic tissue characterization using electrical impedance spectroscopy. Ann. NY Acad. Sci. 873, 51-58 (1999).
4. da Silva JE, de Sa JP, Jossinet J. Classification of breast tissue by electrical impedance spectroscopy. Med. Biol. Eng. Comput. 38, 26-30 (2000).
5. Kyle AH, Chan CT, Minchinton AI. Characterization of three-dimensional tissue cultures using electrical impedance spectroscopy. Biophys. J. 76, 2640-2648(1999).
6. Amirudin A, Thierry D. Application of electrochemical impedance spectroscopy to study the degradation of polymercoated metals. Prog. Org. Coat. 26, 1-28 (1995).
7. Drexler J, Steinem C. Pore-suspending lipid bilayers on porous alumina investigated by electrical impedance spectroscopy. J. Phys. Chem. B. 107, 11245-11254 (2003).
8. Chilcott TC, Chan M, Gaedt L, Nantawisarakul T, Fane AG, Coster HGL. Electrical impedance spectroscopy characterisation of conducting membranes: I. Theory. J. Memb. Sci. 195, 153-167 (2002).
9. Lanfredi S, Rodrigues ACM. Impedance spectroscopy study of the electrical conductivity and dielectric constant of polycrystalline LiNbO3. J. Appl. Phys. 86, 2215-2219 (1999).
10. Schwan HP. Electrical properties of blood and its constitutents: alternating current spectroscopy. Ann. Hematol. 46, 185-197 (1983).
11. McGuinness R. Impedance-based cellular assay technologies: recent advances, future promise. Curr. Opin. Pharmacol. 7, 535-540 (2007).
12. Giaever IC. Keese R. Micromotion of mammalian cells measured electrically. Proc. Natl Acad. Sci. USA 88, 7896-7900 (1991).
13. Zudaire E, Cuesta N, Murty V et al. The aryl hydrocarbon receptor repressor is a putative tumor suppressor gene in multiple human cancers. J. Clin. Invest. 118, 640-650 (2008).
14. Charrier L, Yan YH, Nguyen TT et al. ADAM-15/metargidin mediates homotypic aggregation of human T lymphocytes and heterotypic interactions of T lymphocytes with intestinal epithelial cells. J. Biol. Chem. 282, 16948-16958 (2007).
15. Saxena NK, Sharma D, Ding XL et al. Concomitant activation of the JAK/STAT, P13K/AKT and ERK signaling is involved in leptin-mediated promotion of invasion and migration of hepatocellular carcinoma cells. Cancer Res. 2497-2507 (2007).
16. Alocilja R. Design and fabrication of a microimpedance biosensor for bacterial detection. IEEE Sens. J. 4, 434-440 (2004).
17. Varshney M, Li Y. Interdigitated array microelectrodes based impedance biosensors for detection of bacterial cells. Biosens. Bioelectron. 24, 2951-2960 (2009).
18. Wang L, Wang H, Mitchelson K, Yu Z, Cheng J. Analysis of the sensitivity and frequency characteristics of coplanar electrical cell-substrate impedance sensors. Biosens. Bioelectron. 24, 14-21 (2008).
19. Brischwein M, Herrmann S, Vonau W et al. Electric cell-substrate impedance sensing with screen printed electrode structures. Lab. Chip 6, 819-822 (2006).
20. Pan Y, Guo M, Nie Z et al. Selective collection and detection of leukemia cells on a magnet-quartz crystal microbalance system using aptamer-conjugated magnetic beads. Biosens. Bioelectron. 25(7), 1609-1614 (2009).
21. Hewa P, Thamara M, Tannock GA, Mainwaring DE, Harrison S, Fecondo JV. The detection of influenza A and B viruses in clinical specimens using a quartz crystal microbalance. J. Virol. Methods 162(1-2), 14-21 (2009).
22. Chen K, Obinata H, Izumi T. Detection of G protein-coupled receptor-mediated cellular response involved in cytoskeletal rearrangement using surface plasmon resonance. Biosens. Bioelectron. 25(7), 1675-1680 (2010).
23. Wang Y, Zhu X, Wu M, Xia N, Wang J, Zhou F. Simultaneous and label-free determination of wild-type and mutant p53 at a single surface plasmon resonance chip preimmobilized with consensus DNA and monoclonal antibody. Anal. Chem. 1813-1823 (2009).
24. Fritz J. Cantilever biosensors. Analyst 133, 855-863 (2008).
25. Bouafsoun A, Helali S, Mebarek S et al. Electrical probing of endothelial cell behaviour on a fibronectin/polystyrene/ thiol/gold electrode by Faradaic electrochemical impedance spectroscopy (EIS). Bioelectrochemistry 70, 401-407 (2007).
26. Bouafsoun A, Helali S, Othmane A et al. Evaluation of endothelial cell adhesion onto different protein/gold electrodes by EIS. Macromol. Biosci. 7, 599-610 (2007).
27. Li J, Thielemann C, Reuning U, Johannsmann D. Monitoring of integrinmediated adhesion of human ovarian cancer cells to model protein surfaces by quartz crystal resonators: evaluation in the impedance analysis mode. Biosens. Bioelectron. 20, 1333-1340 (2005).
28. Jiang WG, Ablin RJ, Kynaston HG, Mason MD. The prostate transglutaminase (TGase-4, TGaseP) regulates the interaction of prostate cancer and vascular endothelial cells, a potential role for the ROCK pathway. Microvasc. Res. 77, 150-157 (2009).
29. Chen J, Ye L, Zhang L, Jiang WG. Placenta growth factor, PLGF, influences the motility of lung cancer cells, the role of Rho associated kinase, Rock1. J. Cell. Biochem. 105, 313-320 (2008).
30. Prodan E, Prodan C, Miller JH Jr. The dielectric response of spherical live cells in suspension: an analytic solution. Biophys. J. 95, 4174-4182 (2008).
31. Xiao C, Luong JH. Assessment of cytotoxicity by emerging impedance spectroscopy. Toxicol. Appl. Pharmacol. 206, 102-112 (2005).
32. Keshtkar A, Keshtkar A, Smallwood RH. Electrical impedance spectroscopy and the diagnosis of bladder pathology. Physiol. Meas. 27, 585-596 (2006).
33. Tijero M, Gabriel G, Caro J et al. SU-8 microprobe with microelectrodes for monitoring electrical impedance in living tissues. Biosens. Bioelectron. 24, 2410-2416 (2009).
34. Xiao C, Luong JH. A simple mathematical model for electric cell-substrate impedance sensing with extended applications. Biosens. Bioelectron. 25, 1774-1780 (2010).
35. Hug TS. Biophysical methods for monitoring cell-substrate interactions in drug discovery. Assay Drug Dev. Technol. 1, 479-488 (2003).
36. Rahman AR, Lo CM, Bhansali S. A detailed model for high-frequency impedance characterization of ovarian cancer epithelial cell layer using ECIS electrodes. IEEE Trans. Biomed. Eng. 56, 485-492 (2009).
37. Foster K, Schwan H. Dielectric properties of tissues and biological materials: a critical review. Crit. Rev. Biomed. Eng. 17, 25-104 (1989).
38. Sun T, Bernabini C, Morgan H. Singlecolloidal particle impedance spectroscopy: complete equivalent circuit analysis of polyelectrolyte microcapsules. Langmuir 26, 3821-3828 (2010).
39. Pethig R, Markx GH. Applications of dielectrophoresis in biotechnology. Trends Biotechnol. 15, 426-432 (1997).
40. Owicki JC, Parce JW. Biosensors based on the energy metabolism of living cells: the physical chemistry and cell biology of extracellular acidification. Biosens. Bioelectron. 7, 255-272 (1992).
41. Colquhoun D. Ion channels: this years Nobel prize in physiology or medicine. BMJ 303, 938-939 (1991).
42. Richard S, Lory P, Bourinet E, Nargeot J. Molecular physiology of human cardiovascular ion channels: from electrophysiology to molecular genetics. Meth. Enzymol. 293, 71-88 (1998).
43. Nishida H, Matsumoto A, Tomono N, Hanakai T, Harada S, Nakaya H. Biochemistry and physiology of mitochondrial ion channels involved in cardioprotection. FEBS Lett. 584(10), 2161-2166 (2009).
44. Banales JM, Gradilone SA. Primers on molecular pathways - ion channels: key regulators of pancreatic physiology. Pancreatology 9, 556-559 (2009).
45. Dunne MJ, Petersen OH. Potassium selective ion channels in insulin-secreting cells: physiology, pharmacology and their role in stimulus-secretion coupling. Biochim. Biophys. Acta 1071, 67-82 (1991).
46. Han A, Frazier AB. Ion channel characterization using single cell impedance spectroscopy. Lab. Chip 6, 1412-1414 (2006).
47. Neher E, Sakmann B. The patch clamp technique. Sci. Am. 266, 44-51 (1992)
48. Okada Y, Kohara M. [Principle and practice of patch-clamp technique]. Nippon. Seirigaku. Zasshi. 56, 133-145 (1994).
49. Walker K, Ripandelli N, Flint S. Rapid enumeration of Bifidobacterium lactis in milk powders using impedance. Int. Dairy J. 15, 183-188 (2005).
50. Gomez R, Bashir R, Bhunia AK. Microscale electronic detection of bacterial metabolism. Sens. Actuators B. Chem. 86, 198-208 (2002).
51. Yang L. Electrical impedance spectroscopy for detection of bacterial cells in suspensions using interdigitated microelectrodes. Talanta 74, 1621-1629 (2008).
52. Yang L, Li Y, Griffis CL, Johnson MG. Interdigitated microelectrode (IME) impedance sensor for the detection of viable Salmonella typhimurium. Biosens. Bioelectron. 19, 1139-1147 (2004).
53. Varshney M, Li Y. Double interdigitated array microelectrode-based impedance biosensor for detection of viable Escherichia coli O157: H7 in growth medium. Talanta 74, 518-525 (2008).
54. Yang L, Bashir R. Electrical/ electrochemical impedance for rapid detection of foodborne pathogenic bacteria. Biotechnol. Adv. 26(2), 135-150 (2008).
55. Pnke O, Balkenhohl T, Kafka J, Schfer D, Lisdat F. Impedance spectroscopy and biosensing. Biosensing for the 21st Century, 195-237 (2008).
56. Park G, Choi CK, English AE, Sparer TE. Electrical impedance measurements predict cellular transformation. Cell Biol. Int. 33, 429-433 (2009).
57. Price DT, Rahman RA, Bhansali S. Design rule for optimization of microelectrodes used in electric cell-substrate impedance sensing (ECIS). Biosens. Bioelectron. 24, 2071-2076 (2009).
58. Wegener J, Keese CR, Giaever I. Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces. Exp. Cell Res. 259, 158-166 (2000).
59. Xiao C, Lachance B, Sunahara G, Luong JH. An in-depth analysis of electric cell-substrate impedance sensing to study the attachment and spreading of mammalian cells. Anal. Chem. 74, 1333-1339 (2002).
60. Goda N, Kataoka N, Shimizu J et al. Evaluation of micromotion of vascular endothelial cells in electrical cell-substrate impedance sensing (ECIS) method using a mathematical model. J. Mech. Med. Biol. 5, 357-268 (2005).
61. Guo M, Chen J, Yun X, Chen K, Nie L, Yao S. Monitoring of cell growth and assessment of cytotoxicity using electrochemical impedance spectroscopy. Biochim. Biophys. Acta 1760, 432-439 (2006).
62. Ceriotti L, Ponti J, Colpo P, Sabbioni E, Rossi F. Assessment of cytotoxicity by impedance spectroscopy. Biosens. Bioelectron. 22, 3057-3063 (2007).
63. Male KB, Lachance B, Hrapovic S, Sunahara G, Luong JH. Assessment of cytotoxicity of quantum dots and gold nanoparticles using cell-based impedance spectroscopy. Anal. Chem. 80, 5487-5493 (2008).
64. Ponti J, Ceriotti L, Munaro B et al. Comparison of impedance-based sensors for cell adhesion monitoring and in vitro methods for detecting cytotoxicity induced by chemicals. Altern. Lab. Anim. 34, 515-525 (2006).
65. Glamann J, Hansen AJ. Dynamic detection of natural killer cell-mediated cytotoxicity and cell adhesion by electrical impedance measurements. Assay Drug Dev. Technol. 4, 555-563 (2006).
66. Xiao C, Luong JH. On-line monitoring of cell growth and cytotoxicity using electric cell-substrate impedance sensing (ECIS). Biotechnol. Prog. 19, 1000-1005 (2003).
67. Yeon JH, Park JK. Cytotoxicity test based on electrochemical impedance measurement of HepG2 cultured in microfabricated cell chip. Anal. Biochem. 341, 308-315 (2005).
68. Male KB, Rao YK, Tzeng YM, Montes J, Kamen A, Luong JH. Probing inhibitory effects of Antrodia camphorata isolates using insect cell-based impedance spectroscopy: inhibition vs chemical structure. Chem. Res. Toxicol. 21, 2127-2133 (2008).
69. Male KB, Tzeng YM, Montes J et al. Probing inhibitory effects of destruxins from metarhizium anisopliae using insect cell based impedance spectroscopy: inhibition vs chemical structure. Analyst 134, 1447-1452 (2009).
70. Male KB, Lachance B, Hrapovic S, Sunahara G, Luong JHT. Assessment of cytotoxicity of quantum dots and gold nanoparticles using cell-based impedance spectroscopy. Anal. Chem. 80, 5487-5493 (2008).
71. Curtis TM, Tabb J, Romeo L, Schwager SJ, Widder MW, van der Schalie WH. Improved cell sensitivity and longevity in a rapid impedance-based toxicity sensor. J. Appl. Toxicol. 29, 374-380 (2009).
72. Asphahani F, Zhang M. Cellular impedance biosensors for drug screening and toxin detection. Analyst 132, 835-841 (2007).
73. Yin H, Wang FL, Wang AL, Cheng J, Zhou Y. Bioelectrical impedance assay to monitor changes in aspirin-treated human colon cancer HT-29 cell shape during apoptosis. Anal. Lett. 40, 85-94 (2007).
74. Arias RL, Perry CA, Yang L. Real-time electrical impedance detection of cellular activities of oral cancer cells. Biosens. Bioelectron. 25(10), 2225-2231 (2010).
75. Lee JF, Zeng Q, Ozaki H et al. Dual roles of tight junction-associated protein, zonula occludens-1, in sphingosine 1-phosphatemediated endothelial chemotaxis and barrier integrity. J. Biol. Chem. 281, 29190-29200 (2006).
76. Kucharzik T, Lugering A, Yan Y et al. Activation of epithelial CD98 glycoprotein perpetuates colonic inflammation. Lab. Invest. 85, 932-941 (2005).
77. Charrier L, Yan Y, Driss A, Laboisse CL, Sitaraman SV, Merlin D. ADAM-15 inhibits wound healing in human intestinal epithelial cell monolayers. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G346-G353 (2005).
78. Earley S, Plopper GE. Disruption of focal adhesion kinase slows transendothelial migration of AU-565 breast cancer cells. Biochem. Biophys. Res. Commun. 350, 405-412 (2006).
79. Leung G, Tang HR, McGuinness R, Verdonk E, Michelotti JM, Liu VF. Cellular dielectric spectroscopy: a label-free technology for drug discovery. JALA Charlottesv Va. 10, 258-269 (2005).
80. Mancuso L, Liuzzo MI, Fadda S et al. In vitro ovine articular chondrocyte proliferation: experiments and modelling. Cell Prolif. 43, 310-320 (2010).
81. Bryan AK, Goranov A, Amon A, Manalis SR. Measurement of mass, density, volume during the cell cycle of yeast. Proc. Natl Acad. Sci. USA 107(3), 999-1004 (2010).
82. Gawad S, Schild L, Renaud PH. Micromachined impedance spectroscopy flow cytometer for cell analysis and particle sizing. Lab. Chip 1, 76-82 (2001).
83. Lowe W. Understanding disuse atrophy. Massage Today 5, 10 (2005) 84 Zeng H, Zhao Y. Rheological analysis of non-newtonian blood flow using a microfluidic device. Sens. Actuators A Phys. DOI: 10.1016/j.sna.2010.01.031 (2010) (In press).
84. Cho S, Thielecke H. Micro hole-based cell chip with impedance spectroscopy. Biosens. Bioelectron. 22, 1764-1768 (2007).
85. Jang LS, Wang MH. Microfluidic device for cell capture and impedance measurement. Biomed. Microdevices 9, 737-743 (2007).
86. Ayliffe HE, Frazier AB, Rabbitt RD. Electric impedance spectroscopy using microchannels with integrated metal electrodes. J. Microelectromech. Syst. 8, 50-57 (1999).
87. Suehiro J, Hamada R, Noutomi D, Shutou M, Hara M. Selective detection of viable bacteria using dielectrophoretic impedance measurement method. J. Electrostat. 57, 157-168 (2003).
88. Iliescu C, Poenar DP, Carp M, Loe FC. A microfluidic device for impedance spectroscopy analysis of biological samples. Sens. Actuators B. Chem. 123, 168-176 (2007).
89. Gomez-Sjoberg R, Morisette DT, Bashir R. Impedance microbiology-on-a- chip: Microfluidic bioprocessor for rapid detection of bacterial metabolism. J. Microelectromech. Syst. 14, 829-838 (2005).
90. Medoro G, Manaresi N, Leonardi A, Altomare L, Tartagni M, Guerrieri R. A lab-on-a-chip for cell detection and manipulation. IEEE Sens. J. 3, 317-325 (2005).
91. Wu J, Ben YX, Battigelli D, Chang HC. Long-range AC electroosmotic trapping and detection of bioparticles. Ind. Eng. Chem. Res. 44, 2815-2822 (2005).
92. Minerick AR, Zhou R, Takhistov P, Chang HC. Manipulation and characterization of red blood cells with alternating current fields in microdevices. Electrophoresis 24, 3703-3717 (2003).
93. Ichiki T, Shinbashi S, Ujiie T, Horiike Y. Microchip technologies for the analysis of biological cells. J. Photopolym. Sci. Technol. 15, 487-492 (2002).
94. Yang M, Lim CC, Liao R, Zhang X. A novel microfluidic impedance assay for monitoring endothelin-induced cardiomyocyte hypertrophy. Biosens. Bioelectron. 22, 1688-1693 (2007).
95. Gascoyne PR, Vykoukal JV. Dielectrophoresis-based sample handling in general-purpose programmable diagnostic instruments. Proc. IEEE Inst. Electr. Electron Eng. 92, 22-42 (2004).
96. Liu YS, Walter TM, Chang WJ et al. Electrical detection of germination of viable model Bacillus anthracis spores in microfluidic biochips. Lab. Chip 7, 603-610 (2007).
97. Suehiro J, Hatano T, Shutou M, Hara M. Improvement of electric pulse-shape for electropermeabilizationassisted dielectrophoretic impedance measurement for high sensitive bacteria detection. Sens. Actuators B Chem. 109, 209-215 (2005).
98. Holmes D, Pettigrew D, Reccius CH et al. Leukocyte analysis and differentiation using high speed microfluidic single cell impedance cytometry. Lab. Chip 9, 2881-2889 (2009).
99. Watkins N, Venkatesan BM, Toner M, Rodriguez W, Bashir R. A robust electrical microcytometer with 3-dimensional hydrofocusing. Lab. Chip 9, 3177-3184 (2009).
100. Mishra NN, Retterer S, Zieziulewicz TJ et al. On-chip micro-biosensor for the detection of human CD4(+) cells based on AC impedance and optical analysis. Biosens. Bioelectron. 21, 696-704 (2005).
101. Boehm DA, Gottlieb PA, Hua ZS. On-chip microfluidic biosensor for bacterial detection and identification. Sens. Actuators B. Chem. 126, 508-514 (2007).
102. Hon KB, Li L, Hutchings IM. Direct writing technology - advances and developments. CIRP Ann. Manuf. Technol. 57, 601-620 (2008).