Applied Microbiology and Biotechnology

, Volume 103, Issue 19, pp 7917–7929 | Cite as

Pulsed electric field inactivation of microorganisms: from fundamental biophysics to synergistic treatments

  • Allen L. GarnerEmail author


The growth of antibiotic resistant microorganisms and the increasing demand for nonthermal antimicrobial treatment in the food and beverage industry motivates research into alternative inactivation methods. Pulsed electric fields (PEFs) provide an athermal method for inactivating microorganisms by creating nanometer-sized membrane pores in microorganisms, inducing cell death when the PEF duration and intensity are sufficient such that the pores cannot reseal after the PEFs through a process referred to as irreversible electroporation. While PEF inactivation has been studied for several decades, recent studies have focused on extending the technique to various liquids in the food industry and optimizing microorganism inactivation while minimizing adverse effects to the treated sample. This minireview will assess the biophysical mechanisms and theory of PEF-induced cellular interactions and summarize recent advances in applying this technology for microorganism inactivation alone and synergistically in combination with other technologies, including temperature, pressure, natural ingredients, and pharmaceuticals.


Electroporation Microorganism inactivation Applied microbiology Antimicrobial resistance 


Compliance with ethical standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Asami K, Hanai T, Koizumi N (1980) Dielectric approach to suspensions of ellipsoidal particles covered with a shell in particular reference to biological cells. Jpn J Appl Phys 19:359–365Google Scholar
  2. Berdejo D, Pagán E, García-Gonzalo D, Pagán R (2018) Exploiting the synergism among physical and chemical processes for improving food safety. Curr Opin Food Sci 30:14–20Google Scholar
  3. Bresme F, Lervik A, Bedeaux D, Kjelstrup S (2008) Water polarization under thermal gradients. Phys Rev Lett 101:020602Google Scholar
  4. Caminiti IM, Noci F, Muñoz A, Whyte P, Morgan DJ, Cronin DA, Lyng JG (2011) Impact of selected combinations of non-thermal processing technologies on the quality of an apple and cranberry juice blend. Food Chem 124(4):1387–1392Google Scholar
  5. Cemazar M, Sersa G, Frey W, Miklavcic D, Teissié J (2018) Recommendations and requirements for reporting on applications of electric pulse delivery for electroporation of biological samples. Bioelectrochemistry 122:69–76Google Scholar
  6. Chen C, Smye SW, Robinson MP, Evans JA (2006) Membrane electroporation theories: a review. Med Biol Eng Comput 44:5–14Google Scholar
  7. Coustets M, Ganeva V, Galutzov B, Teissie J (2015) Millisecond duration pulses for flow-through electro-induced protein extraction from E. coli and associated eradication. Bioelectrochemistry 103:82–91Google Scholar
  8. Cregenzán-Alberti O, Arroyo C, Dorozko A, Whyte P, Lyng JG (2017) Thermal characterization of Bacillus subtilis endospores and a comparative study of their resistance to high temperature pulsed electric fields (HTPEF) and thermal-only treatments. Food Control 73:1490–1498Google Scholar
  9. Croce RP, De Vita A, Pierro V, Pinto IM (2010) A thermal model for pulsed EM field exposure effects in cells at nonthermal levels. IEEE Trans Plasma Sci 38:149–155Google Scholar
  10. Delemotte L, Tarek M (2012) Molecular dynamics simulations of lipid membrane electroporation. J Membr Biol 245(9):531–543Google Scholar
  11. Edd JF, Horowitz L, Davalos RV, Mir LM, Rubinsky B (2006) In vivo results of a new focal tissue ablation technique: irreversible electroporation. IEEE Trans Biomed Eng 53:1409–1415Google Scholar
  12. Edelblute CM, Hornef J, Burcus NI, Norman T, Beebe SJ, Schoenbach K, Heller R, Jiang C, Guo S (2017) Controllable moderate heating enhances the therapeutic efficacy of irreversible electroporation for pancreatic cancer. Sci Rep 7:11767Google Scholar
  13. Emanuel E, Roman P, Cahan R (2019) Influence of the current density in moderate pulsed electric fields on P. putida F1 eradication. Bioelectrochemistry 126:172–179Google Scholar
  14. Evrendilek GA, Zhang QH, Richter ER (1999) Inactivation of Escherichia coli O157: H7 and Escherichia coli 8739 in apple juice by pulsed electric fields. J Food Prot 62:793–796Google Scholar
  15. Fernández ML, Marshall G, Sagués F, Reigada R (2010) Structural and kinetic molecular dynamics study of electroporation in cholesterol-containing bilayers. J Phys Chem B 114:6855–6865Google Scholar
  16. Friend AW, Gartner SL, Foster KR, Howe H (1981) The effects of high power microwave pulses on red blood cells and the relationship to transmembrane thermal gradients. IEEE Trans Microw Theory Tech 9:1271–1277Google Scholar
  17. Frieri M, Kumar K, Boutin A (2017) Antibiotic resistance. J Infect Public Health 10:369–378Google Scholar
  18. Gabrić D, Barba F, Roohinejad S, Gharibzahedi SMT, Radojčin M, Putnik P, Bursać Kovačević D (2018) Pulsed electric fields as an alternative to thermal processing for preservation of nutritive and physicochemical properties of beverages: a review. J Food Process Eng 41:e12638Google Scholar
  19. Garner AL, Chen N, Yang J, Kolb J, Swanson RJ, Loftin KC, Beebe SJ, Joshi RP, Schoenbach KH (2004) Time domain dielectric spectroscopy measurements of HL-60 cell suspensions after microsecond and nanosecond electrical pulses. IEEE Trans Plasma Sci 32:2073–2084Google Scholar
  20. Garner AL, Chen G, Chen N, Sridhara V, Kolb JF, Swanson RJ, Beebe SJ, Joshi RP, Schoenbach KH (2007) Ultrashort electric pulse induced changes in cellular dielectric properties. Biochem Biophys Res Commun 362:139–144Google Scholar
  21. Garner AL, Deminksy M, Neculaes VB, Chashihin V, Knizhnik A, Potapkin B (2013) Cell membrane thermal gradients induced by electromagnetic fields. J Appl Phys 113:214709Google Scholar
  22. Garner AL, Neculaes VB, Deminsky M, Dylov DV, Joo C, Loghin ER, Yazdanfar S, Conway KR (2016) Plasma membrane temperature gradients and multiple cell permeabilization induced by low peak power density femtosecond lasers. Biochem Biophys Rep 5:168–174Google Scholar
  23. Garner AL, Frelinger AL III, Gerrits AJ, Gremmel T, Forde EE, Carmichael SL, Michelson AD, Neculaes VB (2019) Using extracellular calcium concentration and electric pulse conditions to tune platelet-rich plasma growth factor release and clotting. Med Hypotheses 125:100–105Google Scholar
  24. Gehl J (2003) Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. Acta Physiol Scand 177:437–447Google Scholar
  25. Giacometti J, Kovačević DB, Putnik P, Gabrić D, Bilušić T, Krešić G, Stulić V, Barba FJ, Chemat F, Barbosa-Cánovas G, Jambrak AR (2018) Extraction of bioactive compounds and essential oils from Mediterranean herbs by conventional and green innovative techniques: A review. Food Res Int 113:245–262Google Scholar
  26. Golberg A, Rubinsky B (2012) Towards electroporation based treatment planning considering electric field induced muscle contractions. Technol Cancer Res Treat 11:189–201Google Scholar
  27. Gupta C, Garg AP, Uniyal RC, Kumari A (2008) Comparative analysis of the antimicrobial activity of cinnamon oil and cinnamon extract on some food-borne microbes. Afr J Microbiol Res 2:247–251Google Scholar
  28. Gusbeth C, Frey W, Volkmann H, Schwartz T, Bluhm H (2009) Pulsed electric field treatment for bacteria reduction and its impact on hospital wastewater. Chemosphere 75:228–233Google Scholar
  29. Hamilton WA, Sale AJH (1967) Effects of high electric fields on microorganisms: II. Mechanism of action of the lethal effect. Biochim Biophys Acta Gen Subj 148:789–800Google Scholar
  30. Hu Q, Joshi RP (2009) Transmembrane voltage analyses in spheroidal cells in response to an intense ultrashort electrical pulse. Phys Rev E 79:011901Google Scholar
  31. Huang K, Jiang T, Wang W, Gai L, Wang J (2014) A comparison of pulsed electric field resistance for three microorganisms with different biological factors in grape juice via numerical simulation. Food Bioprocess Technol 7:1981–1995Google Scholar
  32. Ibey BL, Ullery JC, Pakhomova ON, Roth CC, Semenov I, Beier HT, Tarango M, Xiao S, Schoenbach KH, Pakhomov AG (2014) Bipolar nanosecond electric pulses are less efficient at electropermeabilization and killing cells than monopolar pulses. Biochem Biophys Res Commun 443:568–573Google Scholar
  33. Jiang C, Davalos RV, Bischof JC (2015) A review of basic to clinical studies of irreversible electroporation therapy. IEEE Trans Biomed Eng 62:4–20Google Scholar
  34. Joshi RP, Schoenbach KH (2002) Mechanism for membrane electroporation irreversibility under high-intensity, ultrashort electrical pulse conditions. Phys Rev E 66:052901Google Scholar
  35. Korem M, Goldberg NS, Cahan A, Cohen MJ, Nissenbaum I, Moses AE (2018) Clinically applicable irreversible electroporation for eradication of micro-organisms. Lett Appl Microbiol 67:15–21Google Scholar
  36. Krausz AE, Adler BL, Cabral V, Navati M, Doerner J, Charafeddine RA, Chandra D, Liang H, Gunther L, Clendaniel A, Harper S (2015) Curcumin-encapsulated nanoparticles as innovative antimicrobial and wound healing agent. Nanomedicine 11:195–206Google Scholar
  37. Lambricht L, Lopes A, Kos S, Sersa G, Préat V, Vandermeulen G (2016) Clinical potential of electroporation for gene therapy and DNA vaccine delivery. Expert Opin Drug Deliv 13:295–310Google Scholar
  38. Leistner L, Gorris LG (1995) Food preservation by hurdle technology. Trends Food Sci Technol 6:41–46Google Scholar
  39. Li J, Tan W, Yu M, Lin H (2013) The effect of extracellular conductivity on electroporation-mediated molecular delivery. Biochim Biophys Acta 828:461–470Google Scholar
  40. Mahendran R, Ramanan KR, Barba FJ, Lorenzo JM, López-Fernández O, Munekata PE, Roohinejad S, Sant’Ana AS, Tiwari BK (2019) Recent advances in the application of pulsed light processing for improving food safety and increasing shelf life. Trends Food Sci Technol 88:67–79Google Scholar
  41. Marrink SJ, De Vries AH, Mark AE (2004) Coarse grained model for semiquantitative lipid simulations. J Phys Chem B 108:750–760Google Scholar
  42. Martín-Belloso O, Sobrino-López A (2011) Combination of pulsed electric fields with other preservation techniques. Food Bioprocess Technol 4:954–968Google Scholar
  43. Marx G, Moody A, Bermúdez-Aguirre D (2011) A comparative study on the structure of Saccharomyces cerevisiae under nonthermal technologies: high hydrostatic pressure, pulsed electric fields and thermo-sonication. Int J Food Microbiol 151:327–337Google Scholar
  44. Merla C, Pakhomov AG, Semenov I, Vernier PT (2017) Frequency spectrum of induced transmembrane potential and permeabilization efficacy of bipolar electric pulses. Biochim Biophys Acta 1859:1282–1290Google Scholar
  45. Monfort S, Gayán E, Saldaña G, Puértolas E, Condón S, Raso J, Álvarez I (2010) Inactivation of Salmonella Typhimurium and Staphylococcus aureus by pulsed electric fields in liquid whole egg. Innov Food Sci Emerg Technol 11:306–313Google Scholar
  46. Monfort S, Gayán E, Condón S, Raso J, Álvarez I (2011) Design of a combined process for the inactivation of Salmonella Enteritidis in liquid whole egg at 55 C. Int J Food Microbiol 145:476–482Google Scholar
  47. Monfort S, Saldaña G, Condón S, Raso J, Álvarez I (2012) Inactivation of Salmonella spp. in liquid whole egg using pulsed electric fields, heat, and additives. Food Microbiol S30:393–399Google Scholar
  48. Moody A, Marx G, Swanson BG, Bermúdez-Aguirre D (2014) A comprehensive study on the inactivation of Escherichia coli under nonthermal technologies: High hydrostatic pressure, pulsed electric fields and ultrasound. Food Control 37:305–314Google Scholar
  49. Morales-de La Peña M, Salvia-Trujillo L, Rojas-Graü MA, Martín-Belloso O (2010) Impact of high intensity pulsed electric field on antioxidant properties and quality parameters of a fruit juice–soymilk beverage in chilled storage. LWT Food Sci Technol 43:872–881Google Scholar
  50. Moran JL, Dingari NN, Garcia PA, Buie CR (2018) Numerical study of the effect of soft layer properties on bacterial electroporation. Bioelectrochemistry 123:261–272Google Scholar
  51. Mosqueda-Melgar J, Raybaudi-Massilia RM, Martín-Belloso O (2007) Influence of treatment time and pulse frequency on Salmonella Enteritidis, Escherichia coli and Listeria monocytogenes populations inoculated in melon and watermelon juices treated by pulsed electric fields. Int J Food Microbiol 117:192–200Google Scholar
  52. Mosqueda-Melgar J, Elez-Martinez P, Raybaudi-Massilia RM, Martin-Belloso O (2008a) Effects of pulsed electric fields on pathogenic microorganisms of major concern in fluid foods: a review. Crit Rev Food Sci Nutr 48:747–759Google Scholar
  53. Mosqueda-Melgar J, Raybaudi-Massilia RM, Martín-Belloso O (2008b) Non-thermal pasteurization of fruit juices by combining high-intensity pulsed electric fields with natural antimicrobials. Innov Food Sci Emerg Technol 9:328–340Google Scholar
  54. Napotnik TB, Reberšek M, Vernier PT, Mali B, Miklavčič D (2016) Effects of high voltage nanosecond electric pulses on eukaryotic cells (in vitro): a systematic review. Bioelectrochemistry 110:1–12Google Scholar
  55. Narsetti R, Curry RD, McDonald KF, Clevenger TE, Nichols LM (2006) Microbial inactivation in water using pulsed electric fields and magnetic pulse compressor technology. IEEE Trans Plasma Sci 34:1386–1393Google Scholar
  56. Neu JC, Krassowska W (1999) Asymptotic model of electroporation. Phys Rev E 59:3471–3482Google Scholar
  57. Novac BM, Banakhr FA, Smith IR, Pécastaing L, Ruscassié R, De Ferron AS, Pignolet P (2014) Demonstration of a novel pulsed electric field technique generating neither conduction currents nor Joule effects. IEEE Trans Plasma Sci 42:216–228Google Scholar
  58. Novickij V, Švedienė J, Paškevičius A, Novickij J (2017) In vitro evaluation of nanosecond electroporation against Trichophyton rubrum with or without antifungal drugs and terpenes. Mycoscience 58:261–266Google Scholar
  59. Novickij V, Zinkevičienė A, Perminaitė E, Čėsna R, Lastauskienė E, Paškevičius A, Švedienė J, Markovskaja S, Novickij J, Girkontaitė I (2018a) Non-invasive nanosecond electroporation for biocontrol of surface infections: an in vivo study. Sci Rep 8:14516Google Scholar
  60. Novickij V, Zinkevičienė A, Stanevičienė R, Gruškienė R, Servienė E, Vepštaitė-Monstavičė I, Krivorotova T, Lastauskienė E, Sereikaitė J, Girkontaitė I, Novickij J (2018b) Inactivation of Escherichia coli using nanosecond electric fields and nisin nanoparticles: a kinetics study. Front Microbiol 9:3006Google Scholar
  61. Novickij V, Švedienė J, Paškevičius A, Markovskaja S, Girkontaitė I, Zinkevičienė A, Lastauskienė E, Novickij J (2018c) Pulsed electric field-assisted sensitization of multidrug-resistant Candida albicans to antifungal drugs. Future Microbiol 13:535–546Google Scholar
  62. Nuccitelli R (2018) Application of pulsed electric fields to cancer therapy. Bioelectricity 1:24–28Google Scholar
  63. Pakhomov AG, Kolb JF, White JA, Joshi RP, Xiao S, Schoenbach KH (2007) Long-lasting plasma membrane permeabilization in mammalian cells by nanosecond pulsed electric field (nsPEF). Bioelectromagnetics 28:655–663Google Scholar
  64. Pal M (2017) Pulsed electric field processing: an emerging technology for food preservation. J Exp Food Chem 3:2Google Scholar
  65. Palgan I, Caminiti IM, Muñoz A, Noci F, Whyte P, Morgan DJ, Cronin DA, Lyng JG (2011) Combined effect of selected non-thermal technologies on Escherichia coli and Pichia fermentans inactivation in an apple and cranberry juice blend and on product shelf life. Int J Food Microbiol 151:1–6Google Scholar
  66. Pankaj SK, Keener KM (2017) Cold plasma: Background, applications and current trends. Curr Opin Food Sci 16:49–52Google Scholar
  67. Petrella RA, Schoenbach KH, Xiao S (2016) A dielectric rod antenna for picosecond pulse stimulation of neurological tissue. IEEE Trans Plasma Sci 44:708–714Google Scholar
  68. Piggot TJ, Holdbrook DA, Khalid S (2011) Electroporation of the E. coli and S. aureus membranes: molecular dynamics simulations of complex bacterial membranes. J Phys Chem B 115:13381–13388Google Scholar
  69. Piggot TJ, Piñeiro A, Khalid S (2012) Molecular dynamics simulations of phosphatidylcholine membranes: a comparative force field study. J Chem Theory Comp 8:4593–4609Google Scholar
  70. Pina-Pérez MC, Martínez-López A, Rodrigo D (2012) Cinnamon antimicrobial effect against Salmonella typhimurium cells treated by pulsed electric fields (PEF) in pasteurized skim milk beverage. Food Res Int 48:777–783Google Scholar
  71. Polak A, Bonhenry D, Dehez F, Kramar P, Miklavčič D, Tarek M (2013) On the electroporation thresholds of lipid bilayers: molecular dynamics simulation investigations. J Membr Biol 246:843–850Google Scholar
  72. Probst U, Fuhrmann I, Beyer L (2018) Electrochemotherapy as a new modality in interventional oncology: a review. Technol Cancer Res Treat 17:1–12Google Scholar
  73. Pyatkovskyy TI, Shynkaryk MV, Mohamed HM, Yousef AE, Sastry SK (2018) Effects of combined high pressure (HPP), pulsed electric field (PEF) and sonication treatments on inactivation of Listeria innocua. J Food Eng 233:49–56Google Scholar
  74. Qin S, Timoshkin IV, Maclean M, Wilson MP, Given MJ, Wang T, Anderson JG, MacGregor SJ (2015) Pulsed electric field treatment of Saccharomyces cerevisiae using different waveforms. IEEE Trans Dielectr Electr Insul 22:1841–1848Google Scholar
  75. Qin S, Timoshkin IV, Maclean M, MacGregor SJ, Wilson MP, Given MJ, Wang T, Anderson JG (2016) TiO2-coated electrodes for pulsed electric field treatment of microorganisms. IEEE Trans Plasma Sci 44:2121–2128Google Scholar
  76. Qiu X, Sharma S, Tuhela L, Jia M, Zhang QH (1998) An integrated PEF pilot plant for continuous nonthermal pasteurization of fresh orange juice. Trans ASAE 41:1069–1074Google Scholar
  77. Raso J, Calderón ML, Góngora M, Barbosa-Cánovas G, Swanson BG (1998) Inactivation of mold ascospores and conidiospores suspended in fruit juices by pulsed electric fields. LWT Food Sci Technol 31:668–672Google Scholar
  78. Raso J, Frey W, Ferrari G, Pataro G, Knorr D, Teissie J, Miklavčič D (2016) Recommendations guidelines on the key information to be reported in studies of application of PEF technology in food and biotechnological processes. Innov Food Sci Emerg Technol 37:312–321Google Scholar
  79. Rieder A, Schwartz T, Schön-Hölz K, Marten SM, Süß J, Gusbeth C, Kohnen W, Swoboda W, Obst U, Frey W (2008) Molecular monitoring of inactivation efficiencies of bacteria during pulsed electric field treatment of clinical wastewater. J Appl Microbiol 105:2035–2045Google Scholar
  80. Robinson VS, Garner AL, Loveless AM, Neculaes VB (2017) Calculated plasma membrane voltage induced by applying electric pulses using capacitive coupling. Biomed Phys Eng Express 3:025016Google Scholar
  81. Saldaña G, Monfort S, Condón S, Raso J, Álvarez I (2012) Effect of temperature, pH and presence of nisin on inactivation of Salmonella Typhimurium and Escherichia coli O157: H7 by pulsed electric fields. Food Res Int 45:1080–1086Google Scholar
  82. Sale AJH, Hamilton WA (1967) Effects of high electric fields on microorganisms: I. Killing of bacteria and yeasts. Biochim Biophys Acta Gen Subj 148:781–788Google Scholar
  83. Sale AJH, Hamilton WA (1968) Effects of high electric fields on micro-organisms: III. Lysis of erythrocytes and protoplasts. Biochim Biophys Acta Biomembr 163:37–43Google Scholar
  84. Schoenbach KH, Joshi RP, Kolb JF, Chen N, Stacey M, Blackmore PF, Buescher ES, Beebe SJ (2004) Ultrashort electrical pulses open a new gateway into biological cells. Proc IEEE 92:1122–1137Google Scholar
  85. Schoenbach KH, Xiao S, Joshi RP, Camp JT, Heeren T, Kolb JF, Beebe SJ (2008) The effect of intense subnanosecond electrical pulses on biological cells. IEEE Trans Plasma Sci 36:414–422Google Scholar
  86. Siemer C, Toepfl S, Heinz V (2014) Inactivation of Bacillus subtilis spores by pulsed electric fields (PEF) in combination with thermal energy–I. Influence of process-and product parameters. Food Control 39:163–171Google Scholar
  87. Sitzmann W, Vorobiev E, Lebovka N (2016) Applications of electricity and specifically pulsed electric fields in food processing: historical backgrounds. Innov Food Sci Emerg Technol 37:302–311Google Scholar
  88. Song J, Joshi RP, Schoenbach KH (2011) Synergistic effects of local temperature enhancements on cellular responses in the context of high-intensity, ultrashort electric pulses. Med Biol Eng Comput 49:713–718Google Scholar
  89. Song J, Garner AL, Joshi RP (2017) Molecular dynamics assessment of the role of thermal gradients created by electromagnetic fields on cell membrane electroporation. Phys Rev Appl 7:024003Google Scholar
  90. Teissie J, Rols MP (1993) An experimental evaluation of the critical potential difference inducing cell membrane electropermeabilization. Biophys J 65:409–413Google Scholar
  91. Tieleman DP (2004) The molecular basis of electroporation. BMC Biochem 5:10Google Scholar
  92. Timmermans RA, Groot MN, Nederhoff AL, Van Boekel MA, Matser AM, Mastwijk HC (2014) Pulsed electric field processing of different fruit juices: impact of pH and temperature on inactivation of spoilage and pathogenic micro-organisms. Int J Food Microbiol 173:105–111Google Scholar
  93. Vadlamani A, Detwiler DA, Dhanabal A, Garner AL (2018) Synergistic bacterial inactivation by combining antibiotics with nanosecond electric pulses. Appl Microbiol Biotechnol 102:7589–7596Google Scholar
  94. Van Heesch EJM, Pemen AJM, Huijbrechts PA, van der Laan PC, Prasinski KJ, Zanstra GJ, de Jong P (2000) A fast pulsed power source applied to treatment of conducting liquids and air. IEEE Trans Plasma Sci 28:137–143Google Scholar
  95. Van Impe J, Smet C, Tiwari B, Greiner R, Ojha S, Stulić V, Vukušić T, Režek Jambrak A (2018) State of the art of nonthermal and thermal processing for inactivation of micro-organisms. J Appl Microbiol 125:16–35Google Scholar
  96. Vasilkoski Z, Esser AT, Gowrishankar TR, Weaver JC (2006) Membrane electroporation: the absolute rate equation and nanosecond time scale pore creation. Phys Rev E 74:021904Google Scholar
  97. Vega-Mercado H, Powers JR, Barbosa-Cánovas GV, Swanson BG (1995) Plasmin inactivation with pulsed electric fields. J Food Sci 60:1143–1146Google Scholar
  98. Vega-Mercado H, Martin-Belloso O, Qin BL, Chang FJ, Góngora-Nieto MM, Barbosa-Canovas GV, Swanson BG (1997) Non-thermal food preservation: pulsed electric fields. Trends Food Sci Technol 8:151–157Google Scholar
  99. Vernier PT, Sun Y, Gundersen MA (2006) Nanoelectropulse-driven membrane perturbation and small molecule permeabilization. BMC Cell Biol 7:37Google Scholar
  100. Vernier PT, Levine ZA, Gundersen MA (2013) Water bridges in electropermeabilized phospholipid bilayers. Proc IEEE 101:494–504Google Scholar
  101. Walkling-Ribeiro M, Noci F, Riener J, Cronin DA, Lyng JG, Morgan DJ (2009) The impact of thermosonication and pulsed electric fields on Staphylococcus aureus inactivation and selected quality parameters in orange juice. Food Bioprocess Technol 2:422–430Google Scholar
  102. Walkling-Ribeiro M, Rodríguez-González O, Jayaram SH, Griffiths MW (2011) Processing temperature, alcohol and carbonation levels and their impact on pulsed electric fields (PEF) mitigation of selected characteristic microorganisms in beer. Food Res Int 44:2524–2533Google Scholar
  103. Wang MS, Wang LH, Bekhit AE, Yang J, Hou ZP, Wang YZ, Dai QZ, Zeng XA (2018) A review of sublethal effects of pulsed electric field on cells in food processing. J Food Eng 223:32–41Google Scholar
  104. Wouters PC, Alvarez I, Raso J (2001) Critical factors determining inactivation kinetics by pulsed electric field food processing. Trends Food Sci Technol 12:112–121Google Scholar
  105. Yang N, Huang K, Lyu C, Wang J (2016) Pulsed electric field technology in the manufacturing processes of wine, beer, and rice wine: a review. Food Control 61:28–38Google Scholar
  106. Zhang Q, Zhuang J, von Woedtke T, Kolb JF, Zhang J, Fang J, Weltmann KD (2014) Synergistic antibacterial effects of treatments with low temperature plasma jet and pulsed electric fields. Appl Phys Lett 105:104103Google Scholar
  107. Zhao W, Yang R, Lu R, Wang M, Qian P, Yang W (2008) Effect of PEF on microbial inactivation and physical–chemical properties of green tea extracts. LWT Food Sci Technol 41:425–431Google Scholar
  108. Zhao W, Yang R, Zhang HQ (2012) Recent advances in the action of pulsed electric fields on enzymes and food component proteins. Trends Food Sci Technol 27:83–96Google Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Nuclear EngineeringPurdue UniversityWest LafayetteUSA
  2. 2.Department of Agricultural and Biological EngineeringPurdue UniversityWest LafayetteUSA
  3. 3.School of Electrical and Computer EngineeringPurdue UniversityWest LafayetteUSA

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