Microfluidic Chip with Integrated Electrical Cell-Impedance Sensing for Monitoring Single Cancer Cell Migration in Three-Dimensional Matrixes
Abstract
Cell migration has been recognized as one hallmark of malignant tumor progression. By integrating the method of electrical cell-substrate impedance sensing (ECIS) with the Boyden chamber design, the state-of-the-art techniques provide kinetic information about cell migration and invasion processes in three-dimensional (3D) extracellular matrixes. However, the information related to the initial stage of cell migration with single-cell resolution, which plays a unique role in the metastasis-invasion cascade of cancer, is not yet available. In this paper, we present a microfluidic device integrated with ECIS for investigating single cancer cell migration in 3D matrixes. Using microfluidics techniques without the requirement of physical connections to off-chip pneumatics, the proposed sensor chip can efficiently capture single cells on microelectrode arrays for sequential on-chip 2D or 3D cell culture and impedance measurement. An on-chip single-cell migration assay was successfully demonstrated within several minutes. Migration of single metastatic MDA-MB-231 cells in their initial stage can be monitored in real time; it shows a rapid change in impedance magnitude of approximately 10 Ω/s, whereas no prominent impedance change is observed for less-metastasis MCF-7 cells. The proposed sensor chip, allowing for a rapid and selective detection of the migratory properties of cancer cells at the single-cell level, could be applied as a new tool for cancer research.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Each cell line showed a disparate impedance change, suggesting the biosensor can differentiate between metastatic and nonmetastatic cells.
“Each cell line showed a disparate impedance change, suggesting the biosensor can differentiate between metastatic and nonmetastatic cells.”
From Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors (2014) · cites this paper as [97]
Because the sensor could track single cells in a 3D matrix, functions such as individual cell adhesion, spreading, and migration could be monitored.
“Also, because the sensor could track single cells in a 3D matrix, functions such as individual cell adhesion, spreading, and migration could be monitored. 97”
From Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors (2014) · cites this paper as [97]
Nguyen et al. used electrical cell-substrate impedance sensing to investigate the migration of metastatic and nonmetastatic human mammary gland/breast cells through Matrigel.
“Nguyen et al . 97 used electrical cell-substrate impedance sensing to investigate the migration of metastatic and nonmetastatic human mammary gland/breast cells through Matrigel.”
From Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors (2014) · cites this paper as [97]
Cites
Tumour-cell invasion and migration: diversity and escape mechanisms
Friedl, P., & Wolf, K. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1075 · Cited by 3,225 · see citing works
Mechanics of Motor Proteins and the Cytoskeleton
Howard, & Clark (2002) · Applied Mechanics Reviews · doi:10.1115/1.1451234 · Cited by 2,909 · see citing works
Three-dimensional micro-channel fabrication in polydimethylsiloxane (PDMS) elastomer
Jo, B.-H., Lerberghe, L. M. V., Motsegood, K. M., & Beebe, D. J. (2000) · Journal of Microelectromechanical Systems · doi:10.1109/84.825780 · Cited by 1,098 · see citing works
Micromotion of mammalian cells measured electrically.
Giæver, I., & Keese, C. R. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.17.7896 · Cited by 830 · see citing works
Impedance Characterization and Modeling of Electrodes for Biomedical Applications
Franks, W., Schenker, I., Schmutz, P., & Hierlemann, A. R. (2005) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2005.847523 · Cited by 660 · see citing works
Microfluidic assay for simultaneous culture of multiple cell types on surfaces or within hydrogels
Shin, Y., Han, S., Jeon, J. S., Yamamoto, K., Zervantonakis, I. K., Sudo, R., Kamm, R. D., & Chung, S. (2012) · Nature Protocols · doi:10.1038/nprot.2012.051 · Cited by 617 · see citing works
Monitoring fibroblast behavior in tissue culture with an applied electric field.
Giæver, I., & Keese, C. R. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.12.3761 · Cited by 609 · see citing works
Giampieri, S., Manning, C. S., Hooper, S., Jones, J. L., Hill, C. S., & Sahai, E. A. (2009) · Nature Cell Biology · doi:10.1038/ncb1973 · Cited by 602 · see citing works
A distinctive role for focal adhesion proteins in three-dimensional cell motility
Fraley, S. I., Feng, Y., Krishnamurthy, R., Kim, D. H., Celedon, A., Longmore, G. D., & Wirtz, D. (2010) · Nature Cell Biology · doi:10.1038/ncb2062 · Cited by 587 · see citing works
Even‐Ram, S., & Yamada, K. M. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.08.015 · Cited by 466 · see citing works
Mrksich, M., Chen, C. S., Younan Xia, A., Dike, L. E., Ingber, D. E., & Whitesides, G. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.20.10775 · Cited by 425 · see citing works
A passive pumping method for microfluidic devices
Walker, G. M., & Beebe, D. J. (2002) · Lab on a Chip · doi:10.1039/b204381e · Cited by 421 · see citing works
Application of Real-Time Cell Electronic Sensing (RT-CES) Technology to Cell-Based Assays
Solly, K. J., Wang, X., Xu, X. Y., Strulovici, B., & Zheng, W. (2004) · Assay and Drug Development Technologies · doi:10.1089/adt.2004.2.363 · Cited by 383 · see citing works
Gene expression and the myth of the average cell
Levsky, J. M. (2002) · Trends in Cell Biology · doi:10.1016/s0962-8924(02)00002-8 · Cited by 250 · see citing works
Han, A., Yang, L. P. H., & Frazier, A. B. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1346 · Cited by 220 · see citing works
Cell based biosensors using microelectrodes
Borkholder, D. A. (1998) · Cited by 149 · see citing works
Hong, J.-L., Lan, K.-C., & Jang, L. (2012) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2012.06.046 · Cited by 126 · see citing works
Microfluidic device for cell capture and impedance measurement
Jang, L., & Wang, M.-H. (2007) · Biomedical Microdevices · doi:10.1007/s10544-007-9084-0 · Cited by 125 · see citing works
Impedance studies of bio-behavior and chemosensitivity of cancer cells by micro-electrode arrays
Liu, Q., Yu, J., Xiao, L., Tang, J. C. O., Zhang, Y., Wang, P., & Yang, M. (2008) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2008.07.044 · Cited by 119 · see citing works
Micropatterns of Matrigel for three-dimensional epithelial cultures
Sodunke, T. R., Turner, K. K., Caldwell, S. A., McBride, K. W., Reginato, M. J., & Noh, H. “. (2007) · Biomaterials · doi:10.1016/j.biomaterials.2007.05.021 · Cited by 109 · see citing works
Continuous differential impedance spectroscopy of single cells
Malleo, D., Nevill, J. T., Lee, L. P., & Morgan, H. (2009) · Microfluidics and Nanofluidics · doi:10.1007/s10404-009-0534-2 · Cited by 100 · see citing works
Cultured Neurons Coupled to Microelectrode Arrays: Circuit Models, Simulations and Experimental Data
Sergio Martinoia, A., Massobrio, P., Bove, M., & Massobrio, G. (2004) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2004.826607 · Cited by 92 · see citing works
Real-time, label-free monitoring of cellular invasion and migration with the xCELLigence system
Bird, C., & Kirstein, S. L. (2009) · Nature Methods · doi:10.1038/nmeth.f.263 · Cited by 91 · see citing works
Influence of cell adhesion and spreading on impedance characteristics of cell-based sensors
Asphahani, F., Thein, M., Omid Veiseh, A., Edmondson, D., Kosai, R., Veiseh, M., Xu, J., & Zhang, M. (2008) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2007.11.021 · Cited by 91 · see citing works
Cancer Cell Invasion Is Enhanced by Applied Mechanical Stimulation
Menon, S., & Beningo, K. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017277 · Cited by 89 · see citing works
Breast tumor cell detection at single cell resolution using an electrochemical impedance technique
Arya, S. K., Lee, K. C., Dah'alan, D. B., Daniel, D., & Rahman, A. R. A. (2012) · Lab on a Chip · doi:10.1039/c2lc21174b · Cited by 84 · see citing works
Impedance-based cellular assay technologies: recent advances, future promise
McGuinness, R. (2007) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2007.08.004 · Cited by 83 · see citing works
A microfluidic device for characterizing the invasion of cancer cells in 3‐D matrix
Liu, T., Li, C., Li, H., Zeng, S., Qin, J., & Lin, B. (2009) · Electrophoresis · doi:10.1002/elps.200900289 · Cited by 80 · see citing works
Chaw, K. C., Manimaran, M., Tay, F. E. H., & Swaminathan, S. (2007) · Biomedical Microdevices · doi:10.1007/s10544-007-9071-5 · Cited by 57 · see citing works
Mamouni, J., & Yang, L. (2011) · Biomedical Microdevices · doi:10.1007/s10544-011-9577-8 · Cited by 57 · see citing works
Micro hole-based cell chip with impedance spectroscopy
Cho, S., & Thielecke, H. (2006) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2006.08.028 · Cited by 55 · see citing works
Shin, Y., Kim, H., Han, S., Won, J., Jeong, H. E., Lee, E. S., Kamm, R. D., Kim, J., & Chung, S. H. (2012) · Advanced Healthcare Materials · doi:10.1002/adhm.201200320 · Cited by 38 · see citing works
Single cell mobility and adhesion monitoring using extracellular electrodes
Lind, R., Connolly, P., Wilkinson, C., Breckenridge, L., & Dow, J. (1991) · Biosensors and Bioelectronics · doi:10.1016/0956-5663(91)85023-p · Cited by 35 · see citing works
Cellular electrical impedance spectroscopy: an emerging technology of microscale biosensors
Gu, W., & Zhao, Y. (2010) · Expert Review of Medical Devices · doi:10.1586/erd.10.47 · Cited by 27 · see citing works
Chen, Y., Zhang, J., Wang, Y., Zhang, L., Reboud, J., Tang, K.-C., & Balasubramanian, N. (2007) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2007.12.006 · Cited by 23 · see citing works
Srinivasaraghavan, V., Strobl, J. S., & Agah, M. (2012) · Lab on a Chip · doi:10.1039/c2lc40778g · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Bhatia, S. N., & Ingber, D. E. (2014) · Nature Biotechnology · doi:10.1038/nbt.2989 · Cited by 3,305 · see citing works
Edmondson, R., Broglie, J. J., Adcock, A. F., & Yang, L. (2014) · ASSAY and Drug Development Technologies · doi:10.1089/adt.2014.573 · Cited by 2,515 · see citing works
Advantages and challenges of microfluidic cell culture in polydimethylsiloxane devices
Halldorsson, S., Lucumi, E., Gómez-Sjöberg, R., & Fleming, R. M. T. (2015) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2014.07.029 · Cited by 1,027 · see citing works
The nanoparticle biomolecule corona: lessons learned – challenge accepted?
Docter, D., Westmeier, D., Markiewicz, M., Stolte, S., Knauer, S. K., & Stauber, R. H. (2015) · Chemical Society Reviews · doi:10.1039/c5cs00217f · Cited by 696 · see citing works
A review of impedance measurements of whole cells
Xu, Y., Xie, X., Duan, Y., Wang, L., Cheng, Z., & Cheng, J. (2015) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2015.10.027 · Cited by 426 · see citing works
Cell-based biosensors: Recent trends, challenges and future perspectives
Gupta, N., Renugopalakrishnan, V., Liepmann, D., Paulmurugan, R., & Malhotra, B. D. (2019) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2019.111435 · Cited by 323 · see citing works
Organ-on-a-chip platforms: a convergence of advanced materials, cells, and microscale technologies
Ahadian, S., Civitarese, R., Bannerman, D., Mohammadi, M. H., Lu, R., Wang, E., Davenport‐Huyer, L., Lai, B., Zhang, B., Zhao, Y., et al. (2018) · Advanced Healthcare Materials · doi:10.1002/adhm.201700506 · Cited by 315 · see citing works
Protein bio-corona: critical issue in immune nanotoxicology
Neagu, M. T., Piperigkou, Z., Καραμάνου, Κ., Engin, A. B., Docea, A. O., Constantin, C., Negrei, C., Nikitovic, D., & Tsatsakis, A. M. (2016) · Archives of Toxicology · doi:10.1007/s00204-016-1797-5 · Cited by 235 · see citing works
Biomedical Applications of Microfluidic Devices: A Review
Gharib, G., Bütün, İ., Muganlı, Z., Kozalak, G., Namlı, İ., Sarraf, S. S., Ahmadi, V. E., Toyran, E., van Wijnen, A. J., & Koşar, A. (2022) · Biosensors · doi:10.3390/bios12111023 · Cited by 230 · see citing works
Recent Advances in Application of Biosensors in Tissue Engineering
Hasan, A., Nurunnabi, M., Morshed, M., Paul, A., Polini, A., Kuila, T., Hariri, M. A., Lee, Y.-K., & Jaffa, A. A. (2014) · BioMed Research International · doi:10.1155/2014/307519 · Cited by 194 · see citing works
Recent advances in the use of microfluidic technologies for single cell analysis
Murphy, T. W., Zhang, Q., Naler, L. B., Ma, S., & Lu, C. (2017) · The Analyst · doi:10.1039/c7an01346a · Cited by 156 · see citing works
Microfluidic Organ/Body-on-a-Chip Devices at the Convergence of Biology and Microengineering
Perestrelo, A. R., Águas, A. C., Rainer, A., & Forte, G. (2015) · Sensors · doi:10.3390/s151229848 · Cited by 151 · see citing works
Li, X., Qin, Z., Fu, H., Li, T., Peng, R., Li, Z., Rini, J. M., & Liu, X. (2020) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2020.112672 · Cited by 145 · see citing works
Skin-on-a-chip models: General overview and future perspectives
Risueño, I., Valencia, L., Jorcano, J. L., & Velasco, D. (2021) · APL Bioengineering · doi:10.1063/5.0046376 · Cited by 138 · see citing works
Pan, Y., Hu, N., Wei, X., Gong, L., Zhang, B., Wan, H., & Wang, P. (2018) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2018.09.046 · Cited by 130 · see citing works
Gkatzis, K., Taghizadeh, S., Huh, D., Stainier, D. Y. R., & Bellusci, S. (2018) · European Respiratory Journal · doi:10.1183/13993003.00876-2018 · Cited by 127 · see citing works
Single-Cell Sequencing for Precise Cancer Research: Progress and Prospects
Zhang, X., Marjani, S. L., Hu, Z., Weissman, S. M., Pan, X., & Wu, S. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-1907 · Cited by 122 · see citing works
Conducting Polymer Scaffolds for Hosting and Monitoring 3D Cell Culture
Inal, S., Hama, A., Ferro, M. P., Pitsalidis, C., Oziat, J., Iandolo, D., Pappa, A., Hadida, M., Huerta, M., Marchat, D., et al. (2017) · Advanced Biosystems · doi:10.1002/adbi.201700052 · Cited by 123 · see citing works
A microfluidic dual-well device for high-throughput single-cell capture and culture
Lin, C., Hsiao, Y.-H., Chang, H.-C., Yeh, C.-F., He, C., Salm, E. M., Chen, C., Chiu, I., & Hsu, C. (2015) · Lab on a Chip · doi:10.1039/c5lc00541h · Cited by 115 · see citing works
Feng, Y., Huang, L. J., Zhao, P., Liang, F., & Wang, W. (2019) · Analytical Chemistry · doi:10.1021/acs.analchem.9b04083 · Cited by 113 · see citing works
Two-Dimensional (2D) and Three-Dimensional (3D) Cell Culturing in Drug Discovery
Joseph, J. S., Malindisa, S. T., & Ntwasa, M. M. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.81552 · Cited by 101 · see citing works
Organs-on-chip monitoring: sensors and other strategies
Kilic, T., Navaee, F., Stradolini, F., Renaud, P., & Carrara, S. (2018) · Microphysiological Systems · doi:10.21037/mps.2018.01.01 · Cited by 96 · see citing works
Microfluidic impedance cytometry for single-cell sensing: Review on electrode configurations
Zhu, S., Zhang, X., Zhou, Z., Han, Y., Xiang, N., & Ni, Z. (2021) · Talanta · doi:10.1016/j.talanta.2021.122571 · Cited by 87 · see citing works
Microfluidic co-culture system for cancer migratory analysis and anti-metastatic drugs screening
Mi, S., Du, Z., Xu, Y., Wu, Z., Qian, X., Zhang, M., & Sun, W. (2016) · Scientific Reports · doi:10.1038/srep35544 · Cited by 85 · see citing works
Microfluidic Biochips for Single‐Cell Isolation and Single‐Cell Analysis of Multiomics and Exosomes
Wang, C., Qiu, J., Liu, M., Wang, Y., Yu, Y., Liu, H., Zhang, Y., & Han, L. G. (2024) · Advanced Science · doi:10.1002/advs.202401263 · Cited by 81 · see citing works
Smart Cell Culture Systems: Integration of Sensors and Actuators into Microphysiological Systems
Modena, M. M., Chawla, K., Misun, P. M., & Hierlemann, A. R. (2018) · ACS Chemical Biology · doi:10.1021/acschembio.7b01029 · Cited by 78 · see citing works
A review of the current understanding of nanoparticles protein corona composition
Breznica, P., Koliqi, R., & Daka, A. (2020) · Medicine and Pharmacy Reports · doi:10.15386/mpr-1756 · Cited by 78 · see citing works
Microfluidic technologies for anticancer drug studies
Valente, K. P., Khetani, S., Kolahchi, A. R., Sanati‐Nezhad, A., Suleman, A., & Akbari, M. (2017) · Drug Discovery Today · doi:10.1016/j.drudis.2017.06.010 · Cited by 76 · see citing works
Implications of Three-Dimensional Cell Culture in Cancer Therapeutic Research
Poornima, K. N., Francis, A. P., Hoda, M., Eladl, M. A., Subramanian, S., Veeraraghavan, V. P., El‐Sherbiny, M., Asseri, S. M., Hussamuldin, A. B. A., Surapaneni, K. M., et al. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.891673 · Cited by 77 · see citing works
3D-printed miniaturized fluidic tools in chemistry and biology
Dixit, C. K., Kadimisetty, K., & Rusling, J. F. (2018) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2018.06.013 · Cited by 73 · see citing works
A review on microelectrode array fabrication techniques and their applications
Tanwar, A., Gandhi, H. A., Kushwaha, D., & Bhattacharya, J. (2022) · Materials Today Chemistry · doi:10.1016/j.mtchem.2022.101153 · Cited by 73 · see citing works
Recent Advances in Electrical Impedance Sensing Technology for Single-Cell Analysis
Zhang, Z., Huang, X., Liu, K., Lan, T., Wang, Z., & Zhu, Z. (2021) · Biosensors · doi:10.3390/bios11110470 · Cited by 70 · see citing works
3D Bioprinting and its application to organ-on-a-chip
Park, J. Y., Jang, J., & Kang, H. (2018) · Microelectronic Engineering · doi:10.1016/j.mee.2018.08.004 · Cited by 71 · see citing works
Microfluidic Systems for Cancer Diagnosis and Applications
Akgönüllü, S., Bakhshpour, M., Pişkin, A. K., & Deni̇zli̇, A. (2021) · Micromachines · doi:10.3390/mi12111349 · Cited by 71 · see citing works
A Review on Microfluidics-Based Impedance Biosensors
Chen, Y.-S., Huang, C., Pai, P., Seo, J., & Lei, K. F. (2023) · Biosensors · doi:10.3390/bios13010083 · Cited by 71 · see citing works
Pan, Y., Jiang, D., Gu, C., Qiu, Y. L., Wan, H., & Wang, P. (2020) · Microsystems & Nanoengineering · doi:10.1038/s41378-020-0130-x · Cited by 72 · see citing works
Emerging tumor-on-chips with electrochemical biosensors
Lei, L., Ma, B., Xu, C., & Liu, H. (2022) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2022.116640 · Cited by 69 · see citing works
Single-Cell RNA Sequencing: Technological Progress and Biomedical Application in Cancer Research
Xu, C., Zheng, Y., & Xu, K. (2023) · Molecular Biotechnology · doi:10.1007/s12033-023-00777-0 · Cited by 74 · see citing works
Real-time monitoring of 3D cell culture using a 3D capacitance biosensor
Lee, S., Han, N., Lee, R., Choi, I., Park, Y., Shin, J., & Yoo, K. (2015) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2015.09.005 · Cited by 68 · see citing works
An impedance biosensor for monitoring cancer cell attachment, spreading and drug-induced apoptosis
Nguyen, T. A., Tiberius, B., Pliquett, U. F., & Urban, G. A. (2016) · Sensors and Actuators A Physical · doi:10.1016/j.sna.2016.02.035 · Cited by 65 · see citing works
Self-citationMicrofluidics for research and applications in oncology
Chaudhuri, P. K., Warkiani, M. E., Jing, T., Kenry, K., & Lim, C. T. (2015) · The Analyst · doi:10.1039/c5an00382b · Cited by 62 · see citing works
Wang, X., Liu, A., Xing, Y., Duan, H., Xu, W., Zhou, Q., Wu, H., Chen, C., & Chen, B. (2018) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2018.01.012 · Cited by 62 · see citing works
Li, X., Chen, M., Zhao, S., & Wang, X. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-021-10205-y · Cited by 61 · see citing works
Young, A. T., Rivera, K. R., Erb, P. D., & Daniele, M. A.-A. (2019) · ACS Sensors · doi:10.1021/acssensors.8b01549 · Cited by 61 · see citing works
Soucy, J. R., Bindas, A. J., Koppes, A. N., & Koppes, R. A. (2019) · iScience · doi:10.1016/j.isci.2019.10.052 · Cited by 61 · see citing works
A Review of Electrical Impedance Characterization of Cells for Label-Free and Real-Time Assays
Le, H. T. N., Kim, J., Park, J., & Cho, S. (2019) · BioChip Journal · doi:10.1007/s13206-019-3401-6 · Cited by 57 · see citing works
Microfluidic-Based Multi-Organ Platforms for Drug Discovery
Kolahchi, A. R., Mohtaram, N. K., Modarres, H. P., Mohammadi, M., Geraili, A., Jafari, P., Akbari, M., & Sanati‐Nezhad, A. (2016) · Micromachines · doi:10.3390/mi7090162 · Cited by 56 · see citing works
3D in vitro corneal models: A review of current technologies
Shiju, T. M., de Oliveira, R. C., & Wilson, S. E. (2020) · Experimental Eye Research · doi:10.1016/j.exer.2020.108213 · Cited by 53 · see citing works
Distinguishing skin cancer cells and normal cells using electrical impedance spectroscopy
Zhang, F., Jin, T., Hu, Q., & He, P. (2018) · Journal of Electroanalytical Chemistry · doi:10.1016/j.jelechem.2018.06.021 · Cited by 53 · see citing works
Impedance Imaging of Cells and Tissues: Design and Applications
Bounik, R., Cardes, F., Uluşan, H., Modena, M. M., & Hierlemann, A. R. (2022) · BME Frontiers · doi:10.34133/2022/9857485 · Cited by 49 · see citing works
Zhang, X., Wang, W., Nordin, A. N., Li, F., Jang, S., & Voiculescu, I. (2017) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2017.03.047 · Cited by 49 · see citing works
Zhu, Z., Frey, O., Haandbæk, N., Franke, F., Rudolf, F., & Hierlemann, A. R. (2015) · Scientific Reports · doi:10.1038/srep17180 · Cited by 48 · see citing works
Recent Advances in Monitoring Cell Behavior Using Cell-Based Impedance Spectroscopy
Hassan, Q., Ahmadi, S., & Kerman, K. (2020) · Micromachines · doi:10.3390/mi11060590 · Cited by 48 · see citing works
Abiri, H., Abdolahad, M., Gharooni, M., Hosseini, S. A., Janmaleki, M., Azimi, S., Hosseini, M., & Mohajerzadeh, S. (2015) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2015.01.057 · Cited by 47 · see citing works
Electrical impedance spectroscopy of single cells in hydrodynamic traps
Hasni, A. E., Schmitz, C., Göbbels, K., Bräunig, P., Jahnen‐Dechent, W., & Schnakenberg, U. (2017) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2017.04.019 · Cited by 43 · see citing works
Biosensors to Monitor Cell Activity in 3D Hydrogel-Based Tissue Models
Fedi, A., Vitale, C., Giannoni, P., Caluori, G., & Marrella, A. (2022) · Sensors · doi:10.3390/s22041517 · Cited by 42 · see citing works
Frontier microfluidic techniques for short and long-term single cell analysis
Avesar, J., Arye, T. B., & Levenberg, S. (2014) · Lab on a Chip · doi:10.1039/c4lc00013g · Cited by 42 · see citing works
Oliveira, M., Conceição, P., Kant, K., Ainla, A., & Diéguez, L. (2021) · Cancers · doi:10.3390/cancers13061381 · Cited by 42 · see citing works
Future advances of artificial biosensor technology in biomedical applications
Gaba, S., Chauhan, N., Chandra, R., & Jain, U. (2024) · Talanta Open · doi:10.1016/j.talo.2024.100301 · Cited by 41 · see citing works
Cancer-on-chip: a 3D model for the study of the tumor microenvironment
Cauli, E., Polidoro, M. A., Marzorati, S., Bernardi, C., Rasponi, M., & Lleò, A. (2023) · Journal of Biological Engineering · doi:10.1186/s13036-023-00372-6 · Cited by 41 · see citing works
The predictive link between matrix and metastasis
Barney, L. E., Jansen, L., Polio, S., Galarza, S., Lynch, M. E., & Peyton, S. R. (2016) · Current Opinion in Chemical Engineering · doi:10.1016/j.coche.2016.01.001 · Cited by 38 · see citing works
Lab-on-a-Chip Platforms for Biophysical Studies of Cancer with Single-Cell Resolution
Shukla, V. C., Kuang, T., Senthilvelan, A., Higuita‐Castro, N., Duarte‐Sanmiguel, S., Ghadiali, S. N., & Gallego‐Perez, D. (2018) · Trends in biotechnology · doi:10.1016/j.tibtech.2018.02.007 · Cited by 40 · see citing works
Zhang, Z., Zheng, T., & Zhu, R. (2019) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2019.127326 · Cited by 38 · see citing works
A Review of Advanced Impedance Biosensors with Microfluidic Chips for Single-Cell Analysis
Kim, S., Song, H., Ahn, H., Kim, T., Jung, J.-H., Cho, S. K., Shin, D., Choi, J., Hwang, Y., & Kim, K. (2021) · Biosensors · doi:10.3390/bios11110412 · Cited by 38 · see citing works
Microfluidic Lab-on-a-Chip for Studies of Cell Migration under Spatial Confinement
Sala, F., Ficorella, C., Osellame, R., Käs, J. A., & Vàzquez, R. M. (2022) · Biosensors · doi:10.3390/bios12080604 · Cited by 38 · see citing works
Real-time monitoring of cell protrusion dynamics by impedance responses
Gagliardi, P. A., Puliafito, A., di Blasio, L., Chianale, F., Somale, D., Seano, G., Bussolino, F., & Primo, L. (2015) · Scientific Reports · doi:10.1038/srep10206 · Cited by 38 · see citing works
The bio-corona and its impact on nanomaterial toxicity
Westmeier, D., Chen, C., Stauber, R. H., & Docter, D. (2015) · European Journal of Nanomedicine · doi:10.1515/ejnm-2015-0018 · Cited by 35 · see citing works
Microengineered Organ-on-a-chip Platforms towards Personalized Medicine
Kankala, R. K., Wang, S., & Chen, A. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666190222143542 · Cited by 35 · see citing works
Feedback-controlled microbubble generator producing one million monodisperse bubbles per second
van Elburg, B., Collado‐Lara, G., Bruggert, G., Segers, T., Versluis, M., & Lajoinie, G. P. R. (2021) · Review of Scientific Instruments · doi:10.1063/5.0032140 · Cited by 35 · see citing works
A microchip integrating cell array positioning with in situ single-cell impedance measurement
Guo, X., Zhu, R., & Zong, X. (2015) · The Analyst · doi:10.1039/c5an01193k · Cited by 34 · see citing works
Szydzik, C., Niego, B., Dalzell, G., Knoerzer, M., Ball, F., Nesbitt, W. S., Medcalf, R. L., Khoshmanesh, K., & Mitchell, A. (2016) · RSC Advances · doi:10.1039/c6ra20688c · Cited by 34 · see citing works
Microfluidic-Based Single-Cell Study: Current Status and Future Perspective
Wu, H., Zhu, J., Huang, Y., Wu, D., & Sun, J. (2018) · Molecules · doi:10.3390/molecules23092347 · Cited by 34 · see citing works
A review of bio-impedance devices
Showkat, I., Khanday, F. A., & Beigh, M. R. (2023) · Medical & Biological Engineering & Computing · doi:10.1007/s11517-022-02763-1 · Cited by 37 · see citing works
How Can Chemometrics Improve Microfluidic Research?
Jalali‐Heravi, M., Arrastia, M. V., & Gomez, F. A. (2015) · Analytical Chemistry · doi:10.1021/ac504863y · Cited by 33 · see citing works
Chip modularity enables molecular information access from organ-on-chip devices with quality control
Shang, W., Chen, C., Lo, K., Payne, G. F., & Bentley, W. E. (2019) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2019.05.030 · Cited by 32 · see citing works
Integration of biological systems with electronic-mechanical assemblies
Yi, N., Cui, H., Zhang, L. G., & Cheng, H. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.04.032 · Cited by 30 · see citing works
Microfluidics: Rapid Diagnosis for Breast Cancer
Panesar, S., & Neethirajan, S. R. (2016) · Nano-Micro Letters · doi:10.1007/s40820-015-0079-8 · Cited by 29 · see citing works
Ghorbani, M., Soleymani, H., Hashemzadeh, H., Mortezazadeh, S., Sedghi, M., Shojaeilangari, S., Allahverdi, A., & Naderi‐Manesh, H. (2021) · Scientific Reports · doi:10.1038/s41598-021-95624-0 · Cited by 29 · see citing works
An overview of the biosensing potential of organometallic compounds
Mishra, D. P., Acharya, B., Tripathy, S., Barik, B., & Sahu, P. K. (2023) · Chemical Physics Impact · doi:10.1016/j.chphi.2023.100326 · Cited by 28 · see citing works
Yesilköy, F., Ueno, R., Desbiolles, B. X. E., Grisi, M., Sakai, Y., Kim, B., & Brügger, J. (2016) · Biomicrofluidics · doi:10.1063/1.4942457 · Cited by 28 · see citing works
Arman, S., Tilley, R. D., & Gooding, J. J. (2023) · The Analyst · doi:10.1039/d3an01423a · Cited by 27 · see citing works
Gabardo, C. M., Adams-McGavin, R. C., Fung, B. C., Mahoney, E. J., Fang, Q., & Soleymani, L. (2017) · Scientific Reports · doi:10.1038/srep42543 · Cited by 27 · see citing works
Personalized Drug Efficacy Monitoring Chip
Velasco, V., Joshi, K., Chen, J., & Esfandyarpour, R. (2019) · Analytical Chemistry · doi:10.1021/acs.analchem.9b03291 · Cited by 26 · see citing works
Ugodnikov, A., Persson, H., & Simmons, C. A. (2024) · Lab on a Chip · doi:10.1039/d3lc01027a · Cited by 29 · see citing works
Sensor technologies for quality control in engineered tissue manufacturing
McCorry, M. C., Reardon, K. F., Black, M. R., Williams, C., Babakhanova, G., Halpern, J. M., Sarkar, S., Swami, N. S., Mirica, K. A., Boermeester, S., et al. (2022) · Biofabrication · doi:10.1088/1758-5090/ac94a1 · Cited by 24 · see citing works
Tehrani, F. D., O'Toole, M. D., & Collins, D. J. (2025) · Lab on a Chip · doi:10.1039/d4lc00882k · Cited by 24 · see citing works
In Situ Partial Treatment of Single Cells by Laminar Flow in the “Open Space”
Zhang, Q., Mao, S., Khan, M., Feng, S., Zhang, W., Li, W., & Lin, J. (2018) · Analytical Chemistry · doi:10.1021/acs.analchem.8b05313 · Cited by 24 · see citing works
Organ-on-a-Chip for Drug Screening: A Bright Future for Sustainability? A Critical Review
Feitor, J. F., Brazaca, L. C., Lima, A. M., Ferreira, V. G., Kassab, G., Bagnato, V. S., Carrilho, E., & Cardoso, D. R. (2023) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.2c01454 · Cited by 24 · see citing works
Single-cell analysis based on lab on a chip fluidic system
Valizadeh, A., & Khosroushahi, A. Y. (2015) · Analytical Methods · doi:10.1039/c5ay02029h · Cited by 23 · see citing works
3D cellular invasion platforms: how do paper-based cultures stack up?
Kenney, R. M., Lloyd, C. C., Whitman, N. A., & Lockett, M. R. (2017) · Chemical Communications · doi:10.1039/c7cc02357j · Cited by 23 · see citing works
Noor, J., Chaudhry, A., & Batool, S. (2023) · Cureus · doi:10.7759/cureus.39634 · Cited by 23 · see citing works
Hydrogels as a New Platform to Recapitulate the Tumor Microenvironment
Ermis, M., Çalamak, S., Calibasi‐Kocal, G., Güven, S., Durmus, N. G., Rizvi, I., Hasan, T. G., Hasırcı, N., Hasırcı, V., & Demirci, U. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813339-2.00015-3 · Cited by 24 · see citing works
Rizwan, M., Tse, J. W., Nori, A., Leong, K. W., & Yim, E. K. F. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809880-6.00027-8 · Cited by 22 · see citing works
Jing, B., Luo, Y., Lin, B., Li, J., Wang, Z. A., & Du, Y. (2019) · RSC Advances · doi:10.1039/c9ra02069a · Cited by 22 · see citing works
Jahnke, H., Mewes, A., Zitzmann, F. D., Schmidt, S., Azendorf, R., & Robitzki, A. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-50326-6 · Cited by 21 · see citing works
Design and analysis of microfluidic cell counter using spice simulation
Iqbal, S. M. A., & Butt, N. Z. (2019) · SN Applied Sciences · doi:10.1007/s42452-019-1327-1 · Cited by 20 · see citing works
Yan, X.-X., Liu, W., Yu, Y., & Chen, C. (2015) · Analytical Methods · doi:10.1039/c5ay00661a · Cited by 19 · see citing works
Ivanovska, J., Zlobec, I., Forster, S., Karamitopoulou, E., Dawson, H., Koelzer, V. H., Agaimy, A., Garreis, F., Söder, S., Laqua, W., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.4908 · Cited by 19 · see citing works
Electrical Impedance Monitoring of C2C12 Myoblast Differentiation on an Indium Tin Oxide Electrode
Ilhwan, P., Hong, Y., Jun, Y.-H., Lee, G.-Y., Jun, H., Pyun, J., Choi, J., & Cho, S. (2016) · Sensors · doi:10.3390/s16122068 · Cited by 19 · see citing works
Recent Advances of Biologically Inspired 3D Microfluidic Hydrogel Cell Culture Systems
Ertl, P. (2015) · Cell Biology & Cell Metabolism · doi:10.24966/cbcm-1943/100005 · Cited by 19 · see citing works
- Authors
- Nguyen, T. A., Yin, T.-I., Reyes, D., & Urban, G. A.
- Affiliations
- University of Freiburg (DE)
- Corresponding author
- Nguyen, Tien Anh
- Venue
- Analytical Chemistry
- Publisher
- American Chemical Society (ACS)
- Published
- 2013-11-08
- Volume
- 85
- Issue
- 22
- Pages
- 11068-11076
- ISSN
- 0003-2700 (ISSN-L)
- 1520-6882
- OpenAlex
- W2331001184
- Cited by
- 189
- References
- 36
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 10 · 2023: 18 · 2022: 10 · 2021: 16 · 2020: 14 · 2019: 23 · 2018: 17 · 2017: 16 · 2016: 18 · 2015: 23 · 2014: 7
- FWCI
- 8.82
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Analytical Chemistry (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › Microfluidic and Bio-sensing Technologies
- Physical Sciences › Engineering › Biomedical Engineering › Microfluidic and Capillary Electrophoresis Applications
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Keywords
- electrical cell-substrate impedance sensing, single-cell migration, tumor cell migration, microfluidics, three-dimensional extracellular matrix, metastasis, MDA-MB-231 cells, MCF-7 cells, microelectrode arrays, on-chip cell culture, impedance measurement
- MeSH terms
- Breast Neoplasms, Cell Movement, Electrodes, Female, Humans, Monitoring, Physiologic, Tumor Cells, Cultured, Biosensing Techniques, Electric Impedance, Cell Culture Techniques, Microfluidics, Microchip Analytical Procedures
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review