Tissue electroporation: quantification and analysis of heterogeneous transport in multicellular environments
Open accessAbstract
Although electroporation is gaining increased attention as a technology to enhance clinical chemotherapy and gene therapy of tissues, direct measurements of electroporation-mediated transport in multicellular environments are lacking. In this study, we used multicellular tumor spheroids of DU145 prostate cancer cells as a model tissue to measure the levels and distribution of molecular uptake in a multicellular environment as a function of electrical and other parameters. These measurements, and subsequent analysis, were used to test the hypothesis that cells in a multicellular environment respond to electroporation in a heterogeneous manner that differs from isolated cells in suspension due to differences in cell state, local solute concentration, and local electric field. In support of the hypothesis, molecular uptake was consistently lower for cells within spheroids than cells in dilute suspension and was spatially heterogeneous, with progressively less uptake observed for cells located deeper within spheroid interiors. Reduced uptake and heterogeneity can be explained quantitatively by accounting for the effects of cell size on transmembrane voltage and cell volume, limited extracellular solute reservoir, heterogeneous field strength due to influence of neighboring cells, and diffusional lag times.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Organoids grow into dense and compact structures that impede diffusion, penetration and cellular accumulation of genetic material, making transfection via traditional techniques difficult.
“Moreover, organoids grow into dense and compact structures that impede diffusion, penetration and cellular accumulation of genetic material, which makes transfection via traditional techniques difficult (7–9).”
From Direct transfection of clonal organoids in Matrigel microbeads: a promising approach toward organoid-based genetic screens (2018) · cites this paper as [8]
The Results and discussion (page not available) report a diffusional delay into spheroid interiors and lower calcein uptake by interior cells during electroporation. The experiments concern multicellular spheroids and calcein, not organoids or genetic material; they do not establish that traditional transfection techniques are difficult in organoids. The paper also says the diffusion delay did not explain its uptake results after the longer incubation used for most experiments. (LLM, conf=0.88)
Experimental — accuracy not yet measuredDirect 3D transfection on already formed organoids remains challenging.
“However, direct 3D transfection on already formed organoids remains challenging.”
From Direct transfection of clonal organoids in Matrigel microbeads: a promising approach toward organoid-based genetic screens (2018) · cites this paper as [8]
The Results and discussion section reports that cells in already formed multicellular spheroids took up less calcein during electroporation than isolated cells, particularly deep within the spheroids. This supports a challenge with direct delivery into a 3D structure, but the paper tests calcein uptake in spheroids, not transfection of organoids. (LLM, conf=0.85)
Experimental — accuracy not yet measuredOrganoids are embedded in extracellular matrix, which constitutes a barrier for efficient transfection.
“One limitation is that organoids are embedded in extracellular matrix and grow into compact structures that hinder transfection using traditional techniques.”
From Direct transfection of clonal organoids in Matrigel microbeads: a promising approach toward organoid-based genetic screens (2018) · cites this paper as [8]
The Introduction describes densely packed tumor spheroids surrounded by extracellular matrix, and the Conclusions report lower molecular uptake during electroporation than in isolated cells. But the study examines spheroids, not organoids, and does not establish that extracellular matrix itself is the barrier to transfection. (LLM, conf=0.87)
Experimental — accuracy not yet measuredLipofection and electroporation have been proven relatively inefficient in transfecting 3D cultures, with transfection efficiencies lower than 5% and 20%, respectively.
“However, they have been proven to be relatively inefficient in transfecting 3D cultures with transfection efficiencies lower than 5 and 20%, respectively (7–9).”
From Direct transfection of clonal organoids in Matrigel microbeads: a promising approach toward organoid-based genetic screens (2018) · cites this paper as [8]
The Results and discussion section reports that cells in multicellular spheroids took up fewer molecules after electroporation than isolated cells, supporting a reduced-delivery effect in a 3D culture model. The study measured calcein uptake, not transfection efficiency, and does not establish the claimed below-20% figure or the lipofection figure. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Part of this paper’s reference list could not be split into single entries.
CRC Handbook of Chemistry and Physics
(2014) · doi:10.1201/b17118 · Cited by 57,706 · see citing works
Crank, J. (1956) · CERN Document Server (European Organization for Nuclear Research) · Cited by 18,281 · see citing works
Park, G. S. (1975) · Polymer · doi:10.1016/0032-3861(75)90130-5 · Cited by 15,035 · see citing works
Shapiro, H. M. (2003) · Wiley eBooks · doi:10.1002/0471722731 · Cited by 2,698 · see citing works
Cell and environment interactions in tumor microregions: the multicell spheroid model.
Sutherland, R. M. (1988) · Science · doi:10.1126/science.2451290 · Cited by 1,803 · see citing works
Theory of electroporation: A review
Weaver, J. C., & Chizmadzhev, Y. A. (1996) · Bioelectrochemistry and Bioenergetics · doi:10.1016/s0302-4598(96)05062-3 · Cited by 1,611 · see citing works
Electroporation and Electrofusion in Cell Biology
Neumann, E., Sowers, A. E., & Jordan, C. A. (1989) · Springer eBooks · doi:10.1007/978-1-4899-2528-2 · Cited by 947 · see citing works
Guide to Electroporation and Electrofusion
Chang, D. C., Saunders, J. A., Chassy, B. M., & Sowers, A. E. (1992) · Elsevier eBooks · doi:10.1016/c2009-0-21564-9 · Cited by 640 · see citing works
Therapeutic perspectives of in vivo cell electropermeabilization
Mir, L. M. (2001) · Bioelectrochemistry · doi:10.1016/s0302-4598(00)00112-4 · Cited by 345 · see citing works
Quantitative Study of Electroporation-Mediated Molecular Uptake and Cell Viability
Canatella, P. J., Karr, J. F., Petros, J. A., & Prausnitz, M. R. (2001) · Biophysical Journal · doi:10.1016/s0006-3495(01)76055-9 · Cited by 256 · see citing works
Self-citationElectropermeabilization of cell membranes
Teissié, J., Eynard, N., Gabriel, B., & Rols, M. (1999) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(98)00060-x · Cited by 221 · see citing works
A practical assessment of transdermal drug delivery by skin electroporation
Prausnitz, M. R. (1999) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(98)00063-5 · Cited by 207 · see citing works
Self-citationClinical applications of electrochemotherapy
Heller, R. F., Gilbert, R. A., & Jaroszeski, M. J. (1999) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(98)00067-2 · Cited by 201 · see citing works
Pavlin, M., Pavšelj, N., & Miklavčič, D. (2002) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2002.1001975 · Cited by 178 · see citing works
Growth and Cellular Characteristics of Multicell Spheroids
Sutherland, R. M., & Durand, R. E. (1984) · Recent results in cancer research/Recent Results in Cancer Research · doi:10.1007/978-3-642-82340-4_2 · Cited by 166 · see citing works
Guide to Electroporation and Electrofusion.
Berg, H. (1992) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(92)80073-p · Cited by 160 · see citing works
Demonstration of an extracellular matrix in multicellular tumor spheroids.
Nederman, T., Norling, B., Glimelius, B. L. G., Carlsson, J., & Brunk, U. T. (1984) · PubMed · Cited by 148 · see citing works
Use of Hoechst 33342 for cell selection from multicell systems.
Durand, R. E. (1982) · Journal of Histochemistry & Cytochemistry · doi:10.1177/30.2.6174559 · Cited by 119 · see citing works
Electric Field-Induced Transmembrane Potential Depends on Cell Density and Organizatio
Susil, R. C., Šemrov, D., & Miklavčič, D. (1998) · Electro- and Magnetobiology · doi:10.3109/15368379809030739 · Cited by 118 · see citing works
In vivo gene delivery by electroporation
Jaroszeski, M. J., Gilbert, R., Nicolau, C. S., & Heller, R. F. (1999) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(98)00068-4 · Cited by 100 · see citing works
Electrochemotherapy, Electrogenetherapy, and Transdermal Drug Delivery
Jaroszeski, M. J., Heller, R. F., & Gilbert, R. A. (2000) · Humana Press eBooks · doi:10.1385/1592590802 · Cited by 83 · see citing works
Transdermal transport efficiency during skin electroporation and iontophoresis
Prausnitz, M. R., Lee, C. S., Liu, C. H., Pang, J. C., Singh, T.-P., Langer, R., & Weaver, J. C. (1996) · Journal of Controlled Release · doi:10.1016/0168-3659(95)00121-2 · Cited by 80 · see citing works
Self-citationAnimal Cell Electroporation and Electrofusion Protocols
(1995) · Methods in molecular biology · doi:10.1385/089603304x · Cited by 78 · see citing works
Prediction and optimization of gene transfection and drug delivery by electroporation
Canatella, P., & Prausnitz, M. R. (2001) · Gene Therapy · doi:10.1038/sj.gt.3301547 · Cited by 63 · see citing works
Self-citationUsing light scatter signal to estimate bacterial biovolume by flow cytometry
Bouvier, T. C., Troussellier, M., Anzil, A., Courties, C., & Servais, P. (2001) · Cytometry · doi:10.1002/1097-0320(20010701)44:3 · Cited by 55 · see citing works
Essand, M., Grönvik, C., Hartman, T., & Carlsson, J. (1995) · International Journal of Cancer · doi:10.1002/ijc.2910630315 · Cited by 33 · see citing works
Automated selective dissociation of cells from different regions of multicellular spheroids
Freyer, J. P., & Schor, P. L. (1989) · In Vitro Cellular & Developmental Biology - Plant · doi:10.1007/bf02624405 · Cited by 28 · see citing works
Oxygen Enhancement Ratio in V79 Spheroids
Durand, R. E. (1983) · Radiation Research · doi:10.2307/3576215 · Cited by 22 · see citing works
Demonstration of an extracellular matrix in multicellular tumor spheroids. Cancer Res
Nederman, T., Norling, B., Glimelius, I. C., Carlsson, J., & Brunk, U. T. (1984) · Cited by 20 · see citing works
Flagged first, then by citations
1 of the 30 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Barba, F. J., Parniakov, O., Pereira, S. A., Wiktor, A., Grimi, N., Boussetta, N., Saraiva, J. A., Raso, J., Martín‐Belloso, O., Witrowa‐Rajchert, D., et al. (2015) · Food Research International · doi:10.1016/j.foodres.2015.09.015 · Cited by 781 · see citing works
Effect of Cell Electroporation on the Conductivity of a Cell Suspension
Pavlin, M., Kandušer, M., Reberšek, M., Pucihar, G., Hart, F. X., Magjarevićcacute, R., & Damijan Miklavčič, A. (2005) · Biophysical Journal · doi:10.1529/biophysj.104.048975 · Cited by 292 · see citing works
Tutorial: Electroporation of cells in complex materials and tissue
Rems, L., & Damijan Miklavčič, A. (2016) · Journal of Applied Physics · doi:10.1063/1.4949264 · Cited by 183 · see citing works
Kinetics of Transmembrane Transport of Small Molecules into Electropermeabilized Cells
Pucihar, G., Kotnik, T., Damijan Miklavčič, A., & Teissié, J. (2008) · Biophysical Journal · doi:10.1529/biophysj.108.135541 · Cited by 179 · see citing works
Frandsen, S. K., Gibot, L., Madi, M., Gehl, J., & Rols, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144028 · Cited by 122 · see citing works
Azencott, H. R., Peter, G. F., & Prausnitz, M. R. (2007) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2007.05.008 · Cited by 121 · see citing works
Self-citationElectropermeabilization of dense cell suspensions
Pucihar, G., Kotnik, T., Teissié, J., & Damijan Miklavčič, A. (2007) · European Biophysics Journal · doi:10.1007/s00249-006-0115-1 · Cited by 105 · see citing works
Selective cytotoxicity of intense nanosecond-duration electric pulses in mammalian cells
Ibey, B. L., Pakhomov, A. G., Gregory, B. W., Алексеевна, Х. В., Roth, C. C., Rassokhin, M. A., Bernhard, J. A., Wilmink, G. J., & Pakhomova, O. N. (2010) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2010.07.008 · Cited by 104 · see citing works
Electroporation in Biological Cell and Tissue: An Overview
Kandušer, M., & Damijan Miklavčič, A. (2008) · Food engineering series · doi:10.1007/978-0-387-79374-0_1 · Cited by 104 · see citing works
Hai, A., & Spira, M. E. (2012) · Lab on a Chip · doi:10.1039/c2lc40091j · Cited by 95 · see citing works
Vorobiev, E., & Lebovka, N. (2008) · Food engineering series · doi:10.1007/978-0-387-79374-0_2 · Cited by 97 · see citing works
Faridnia, F., Burritt, D. J., Bremer, P. J., & Oey, I. (2015) · Food Research International · doi:10.1016/j.foodres.2015.08.028 · Cited by 89 · see citing works
Electroporation of cDNA/Morpholinos to targeted areas of embryonic CNS in Xenopus
Falk, J., Drinjákovic, J., Leung, K.-M., Dwivedy, A., Regan, A. G., Piper, M., & Holt, C. E. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-107 · Cited by 89 · see citing works
Antitumor drug delivery in multicellular spheroids by electropermeabilization
Gibot, L., Wasungu, L., Teissié, J., & Rols, M. (2013) · Journal of Controlled Release · doi:10.1016/j.jconrel.2013.01.021 · Cited by 82 · see citing works
Cardiac ablation with pulsed electric fields: principles and biophysics
Sugrue, A. M., Maor, E., Munoz, F. D., Killu, A. M., & Asirvatham, S. J. (2022) · EP Europace · doi:10.1093/europace/euac033 · Cited by 78 · see citing works
Bao, N., Le, T. T., Cheng, J., & Lu, C. (2010) · Integrative Biology · doi:10.1039/b919820b · Cited by 75 · see citing works
Optimal drug and gene delivery in cancer cells by ultrasound-induced cavitation.
Larina, I. V., Evers, B. M., & Esenaliev, R. O. (2005) · PubMed · Cited by 73 · see citing works
A 3D in vitro spheroid model as a way to study the mechanisms of electroporation
Wasungu, L., Escoffre, J.-M., Valette, A., Teissie, J., & Rols, M.-P. (2009) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2009.03.035 · Cited by 58 · see citing works
Čemažar, M., Golzio, M., Serša, G., Escoffre, J., Coer, A., Vidic, S., & Teissié, J. (2011) · Human Gene Therapy · doi:10.1089/hum.2011.073 · Cited by 58 · see citing works
Pulse Electric Field-Assisted Extraction
Vorobiev, E., & Lebovka, N. (2011) · Contemporary food engineering · doi:10.1201/b11241-3 · Cited by 58 · see citing works
Laperrousaz, B., Porte, S., Gerbaud, S., Härmä, V., Kermarrec, F., Hourtane, V., Bottausci, F., Gidrol, X., & Picollet-D’hahan, N. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky030 · Cited by 54 · see citing works
A numerical analysis of multicellular environment for modeling tissue electroporation
Mezeme, M. E., Pucihar, G., Pavlin, M., Brosseau, C., & Damijan Miklavčič, A. (2012) · Applied Physics Letters · doi:10.1063/1.3700727 · Cited by 54 · see citing works
Effect of Thermal and Nonthermal Processing on Textural Quality of Plant Tissues
Kumar, R., Subramanian, V., & Nadanasabapathi, S. (2015) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2014.908348 · Cited by 52 · see citing works
Sachdev, S., Potočnik, T., Rems, L., & Damijan Miklavčič, A. (2021) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2021.107994 · Cited by 51 · see citing works
Optimising non-viral gene delivery in a tumour spheroid model
Mellor, H. R., Davies, L. A., Caspar, H., Pringle, C. R., Hyde, S. C., Gill, D. R., & Callaghan, R. (2006) · The Journal of Gene Medicine · doi:10.1002/jgm.947 · Cited by 49 · see citing works
Resistor–capacitor modeling of the cell membrane: A multiphysics analysis
Brosseau, C., & Sabri, E. (2021) · Journal of Applied Physics · doi:10.1063/5.0033608 · Cited by 48 · see citing works
Luft, C., & Ketteler, R. (2015) · SLAS DISCOVERY · doi:10.1177/1087057115579638 · Cited by 47 · see citing works
Low voltage pulses can induce apoptosis
Matsuki, N., Ishikawa, T., Imai, Y., & Yamaguchi, T. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.04.019 · Cited by 45 · see citing works
Bioelectrodynamics in living organisms
Zhou, S., & Uesaka, M. (2005) · International Journal of Engineering Science · doi:10.1016/j.ijengsci.2005.11.001 · Cited by 45 · see citing works
Mesojednik, S., Pavlin, D., Serša, G., Coer, A., Kranjc, S., Grošel, A., Tevž, G., & Čemažar, M. (2007) · Gene Therapy · doi:10.1038/sj.gt.3302989 · Cited by 42 · see citing works
Chopinet, L., Wasungu, L., & Rols, M. (2011) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2011.04.054 · Cited by 38 · see citing works
Field distribution and DNA transport in solid tumors during electric field-mediated gene delivery.
Henshaw, J., & Yuan, F. (2008) · Journal of Pharmacy and Science · doi:10.1002/jps.21000 · Cited by 40 · see citing works
Schistosoma japonicum: A method for transformation by electroporation
Yuan, X.-S., Shen, J.-L., Wang, X., Wu, X., Liu, D., Dong, H., & Jiang, M.-S. (2005) · Experimental Parasitology · doi:10.1016/j.exppara.2005.08.010 · Cited by 32 · see citing works
Deora, A. A., Diaz, F., Schreiner, R. P., & Rodriguez-Boulan, E. J. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00617.x · Cited by 31 · see citing works
Mossop, B. J., Barr, R. C., Henshaw, J. W., Zaharoff, D. A., & Yuan, F. (2006) · Annals of Biomedical Engineering · doi:10.1007/s10439-006-9151-3 · Cited by 30 · see citing works
Sieni, E., Bazzolo, B., Pieretti, F., Zamuner, A., Tasso, A., Dettin, M., & Conconi, M. T. (2020) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2020.107626 · Cited by 28 · see citing works
The Effect of Electroporation Type Pulsed Electric Fields on DNA in Aqueous Solution
Golberg, A., & Rubinsky, B. (2010) · Technology in Cancer Research & Treatment · doi:10.1177/153303461000900412 · Cited by 27 · see citing works
Pisani, S., Bertino, G., Prina‐Mello, A., Locati, L. D., Mauramati, S., Genta, I., Dorati, R., Conti, B., & Benazzo, M. (2022) · Cancers · doi:10.3390/cancers14215363 · Cited by 22 · see citing works
3D Spheroids’ Sensitivity to Electric Field Pulses Depends on Their Size
Gibot, L., & Rols, M. (2013) · The Journal of Membrane Biology · doi:10.1007/s00232-013-9535-x · Cited by 22 · see citing works
Dermol‐Černe, J., Vidmar, J., Ščančar, J., Uršič, K., Serša, G., & Damijan Miklavčič, A. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.07.021 · Cited by 21 · see citing works
Meglič, S. H., & Pavlin, M. (2010) · The Journal of Membrane Biology · doi:10.1007/s00232-010-9280-3 · Cited by 20 · see citing works
Monfared, Y. K., Mahmoudian, M., Zakeri‐Milani, P., Cecone, C., Hayashi, T., Ishii, K. J., Conde, J., Matencio, A., & Trotta, F. (2023) · Cancers · doi:10.3390/cancers15143748 · Cited by 15 · see citing works
de, A., Bellard, E., Kolosnjaj‐Tabi, J., Golzio, M., & Rols, M. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15031004 · Cited by 14 · see citing works
Wang, L., Wang, Z., Frank, T. G., Brown, S. I., Chudek, S., & Cuschieri, A. (2009) · Nanomedicine · doi:10.2217/nnm.09.6 · Cited by 14 · see citing works
Monfared, Y. K., Mahmoudian, M., Cecone, C., Caldera, F., Haiaty, S., Heidari, H. R., Rahbarghazi, R., Matencio, A., Zakeri‐Milani, P., & Trotta, F. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14122690 · Cited by 13 · see citing works
Cell-cell proximity effects in multi-cell electroporation
Henslee, B. E., Morss, A., Hu, X. T., Lafyatis, G. P., & Lee, L. J. (2014) · Biomicrofluidics · doi:10.1063/1.4893918 · Cited by 13 · see citing works
Pavlin, M., & Miklavcic, D. (2009) · IEEE Transactions on Plasma Science · doi:10.1109/tps.2008.2005292 · Cited by 12 · see citing works
Mass Transfer Phenomena in Electroporation
Golberg, A., & Rubinsky, B. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-415824-5.00012-6 · Cited by 12 · see citing works
Microinjection and electroporation of embryonic kidney explants: An improved method
Alie, T. M., Vrljicak, P., Myburgh, D. B., & Gupta, I. R. (2007) · Kidney International · doi:10.1038/sj.ki.5002329 · Cited by 11 · see citing works
Calcein Release from Cells In Vitro via Reversible and Irreversible Electroporation
Rajeckaitė, V., Jakštys, B., Rafanavičius, A., Maciulevičius, M., Jakutavičiūtė, M., & Šatkauskas, S. (2017) · The Journal of Membrane Biology · doi:10.1007/s00232-017-0005-8 · Cited by 11 · see citing works
Gene electrotransfer: from biophysical mechanisms to in vivo applications
Escoffre, J., Mauroy, C., Portet, T., Wasungu, L., Rosazza, C., Gilbart, Y., Mallet, L., Bellard, E., Golzio, M., Rols, M., et al. (2009) · Biophysical Reviews · doi:10.1007/s12551-009-0022-7 · Cited by 9 · see citing works
Zou, Y., Wang, C., Ruiyun, P., Wang, L., & Hu, X. (2014) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2014.12.002 · Cited by 8 · see citing works
Development of an Acute Method to Deliver Transgenes Into the Brains of Adult Xenopus laevis
Yamaguchi, A., Woller, D. J., & Rodrigues, P. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00092 · Cited by 7 · see citing works
Photochemically enhanced adenoviral transduction in a multicellular environment
Bonsted, A., Engesæter, B. Ø., Høgset, A., & Berg, K. (2006) · Photochemical & Photobiological Sciences · doi:10.1039/b515066c · Cited by 6 · see citing works
Pucihar, G., Kotnik, T., & Damijan Miklavčič, A. (2007) · Springer eBooks · doi:10.1007/978-3-540-73044-6_166 · Cited by 6 · see citing works
Electronic Emulator of Biological Tissue as an Electrical Load during Electroporation
Pirc, E., Balosetti, B., Damijan Miklavčič, A., & Reberšek, M. (2020) · Applied Sciences · doi:10.3390/app10093103 · Cited by 5 · see citing works
Thermophysical properties of frozen parsley: A state diagram representation
Iaccheri, E., Cevoli, C., Rosa, M. D., & Fabbri, A. (2021) · Journal of Food Process Engineering · doi:10.1111/jfpe.13651 · Cited by 5 · see citing works
Optimal parameters of electroporation for gene and tissue
Rodamporn, S. (2012) · Biomedical Engineering International Conference · doi:10.1109/bmeicon.2012.6172070 · Cited by 5 · see citing works
The kinetics of inactivation of spheroidal microbial cells by pulsed electric fieldsPreprint
Lebovka, N., & Vorobiev, E. (2007) · arXiv (Cornell University) · doi:10.48550/arxiv.0704.2750 · Cited by 5 · see citing works
Pucihar, G., & Damijan Miklavčič, A. (2009) · World Congress on Medical Physics and Biomedical Engineering, September 7 - 12, 2009, Munich, Germany · doi:10.1007/978-3-642-03895-2_22 · Cited by 4 · see citing works
Yano, K.-I., Rems, L., Kotnik, T., Damijan Miklavčič, A., Weaver, J. C., Smith, K. C., Son, R. S., Gowrishankar, T. R., Vernier, P. T., Levine, Z. A., et al. (2016) · Springer eBooks · doi:10.1007/978-4-431-56095-1_4 · Cited by 4 · see citing works
Pulsed electric field processing: food pasteurization, tissue treatment, and seed disinfection
Evrendilek, G. A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-90044-7.00014-8 · Cited by 3 · see citing works
Wu, F., Chen, K., Chen, Y., Liu, H., & Yao, C. (2024) · Journal of Applied Physics · doi:10.1063/5.0187891 · Cited by 3 · see citing works
3D Tissue Models to Bridge the Gap Between Cell Culture and Tissue in Assessing Electroporation
Gibot, L. (2016) · Springer eBooks · doi:10.1007/978-3-319-26779-1_16-1 · Cited by 3 · see citing works
Golzio, M., Mazères, S., & Teissié, J. (2009) · Expert Opinion on Drug Delivery · doi:10.1517/17425240903294043 · Cited by 3 · see citing works
3D Culture Models to Assess Tissue Responses to Electroporation
Bulysheva, A. A., & Heller, R. F. (2017) · Springer eBooks · doi:10.1007/978-3-319-26779-1_29-1 · Cited by 3 · see citing works
Gene electrotransfer: from biophysical mechanisms to in vivo applications
Escoffre, J., Mauroy, C., Portet, T., Wasungu, L., Paganin-Gioanni, A., Golzio, M., Teissié, J., & Rols, M. (2009) · Biophysical Reviews · doi:10.1007/s12551-009-0019-2 · Cited by 3 · see citing works
Saha, S., Ishtiaque, M. S., Hossain, M. I., & Alam, M. K. (2023) · International Conference on Electrical, Computer and Communication Engineering · doi:10.1109/ecce57851.2023.10101507 · Cited by 2 · see citing works
Fernandes, P. C., & Pereira, B. J. (2016) · Acta Urológica Portuguesa · doi:10.1016/j.acup.2016.10.001 · Cited by 2 · see citing works
Understanding Electric Fields for Clinical Use
Mahmood, F. (2011) · Springer eBooks · doi:10.1007/978-1-4419-8363-3_4 · Cited by 2 · see citing works
Tao, X.-N., Xiang, X., Liu, H., Zhu, C.-H., Qiu, J., Zhao, H. L., & Liu, K. (2025) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2025.125882 · Cited by 1 · see citing works
3D Culture Models to Assess Tissue Responses to Electroporation
Bulysheva, A. A., & Heller, R. F. (2017) · Springer eBooks · doi:10.1007/978-3-319-32886-7_29 · Cited by 1 · see citing works
Chakravarty, P. (2009) · SMARTech Repository (Georgia Institute of Technology) · Cited by 1 · see citing works
Quantification and control of ultrasound-mediated cell death modes
Hutcheson, J. D. (2008) · SMARTech Repository (Georgia Institute of Technology) · Cited by 1 · see citing works
Electropulsation, an biophysical delivery method for therapy
Teissié, J., & Čemažar, M. (2007) · Springer eBooks · doi:10.1007/978-3-540-73044-6_157
Collagen Gel as Cell Extracellular Environment to Study Gene Electrotransfer
Meglič, S. H., Damijan Miklavčič, A., & Pavlin, M. (2010) · World Congress on Medical Physics and Biomedical Engineering, September 7 - 12, 2009, Munich, Germany · doi:10.1007/978-3-642-13039-7_179
A 3D SPHEROID MODEL AS A PLATFORM TO STUDY NON-VIRAL GENE DELIVERY SYSTEM
Chen, Y. (2015) · D-Scholarship@Pitt (University of Pittsburgh)
Spheroids, A Three-Dimensional Preclinical Model for Electrochemotherapy and Gene Electrotransfer
Kranjc, S., Čemažar, M., & Serša, G. (2015) · World Congress on Medical Physics and Biomedical Engineering, September 7 - 12, 2009, Munich, Germany · doi:10.1007/978-981-287-817-5_44
Tumor electrotransfection progress and prospects: the impact of knowledge about tumor histology
Mesojednik, S., Pavlin, D., Serša, G., Coer, A., Kranjc, S., Grošel, A., Tevž, G., & Čemažar, M. (2007) · Springer eBooks · doi:10.1007/978-3-540-73044-6_150
Roberts, A. S. (2020) · Cornell University Press eBooks · doi:10.7591/cornell/9781501714405.003.0018
3D Tissue Models to Bridge the Gap Between Cell Culture and Tissue in Assessing Electroporation
Gibot, L. (2017) · Springer eBooks · doi:10.1007/978-3-319-32886-7_16
Fernandes, P. C., & Pereira, B. J. (2017) · Acta Urológica Portuguesa · doi:10.24915/aup.33.3.36
Analysis of six stage Marx electroporator circuit based on pulsed parameters
Haldiyan, A., Ghosh, D., & Saluja, N. K. (2022) · AIP conference proceedings · doi:10.1063/5.0086120
Brosseau, C. (2023) · Studies in mechanobiology, tissue engineering and biomaterials · doi:10.1007/978-3-031-37981-9_5
Analytical Approaches of EMB at Multiple Scales
Brosseau, C. (2023) · Studies in mechanobiology, tissue engineering and biomaterials · doi:10.1007/978-3-031-37981-9_4
Sieni, E., Lamberti, P., Polichetti, M., Modestino, M. R., Galluzzi, A., Kralj, S., Kolosnjaj‐Tabi, J., Forzan, M., & Tucci, V. (2026) · Applied Sciences · doi:10.3390/app16147089
- Authors
- Canatella, P. J., Black, M. M., Bonnichsen, D. M., McKenna, C., & Prausnitz, M. R.
- Affiliations
- Georgia Institute of Technology (US)
- Corresponding author
- Prausnitz, Mark R.
- ORCID
- Prausnitz, Mark R.
- Venue
- Biophysical Journal
- Publisher
- Elsevier BV
- Published
- 2004-05
- Volume
- 86
- Issue
- 5
- Pages
- 3260-3268
- ISSN
- 0006-3495 (ISSN-L)
- PMC
- PMC1304191
- OpenAlex
- W2141405401
- Cited by
- 89
- References
- 30
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 5 · 2022: 4 · 2021: 3 · 2020: 4 · 2018: 3 · 2017: 7 · 2016: 4 · 2015: 7 · 2014: 2 · 2013: 3 · 2012: 3
- FWCI
- 4.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biophysical Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Photodynamic Therapy Research Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Plasma Applications and Diagnostics
- Keywords
- electroporation, tumor spheroids, DU145 cells, transmembrane voltage, cell size effects, gene therapy, chemotherapy enhancement, tissue electroporation
- MeSH terms
- Biological Transport, Biophysics, Calibration, Cell Separation, Extracellular Matrix, Flow Cytometry, Humans, Ion Channels, Male, Membrane Potentials, Prostatic Neoplasms, Time Factors, Models, Statistical, Electroporation, Cell Line, Tumor
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
