In vitro antimicrobial effects and mechanisms of direct current air-liquid discharge plasma on planktonic Staphylococcus aureus and Escherichia coli in liquids.

The direct inactivation effects of an atmospheric pressure direct current (DC) air plasma against planktonic Staphylococcus aureus (S. aureus) and Escherichia coli (E. coli) in aqueous solution are investigated in vitro. Upon plasma treatment, extensively analyses on cell culturability, metabolic capacity, membrane integrity, surface morphology, cellular proteins, nucleic acids and intracellular reactive oxygen species (ROS) for both bacterial species were carried out and significant antimicrobial effects observed. Compared with the cellular culturability, a sub-lethal viable but non-culturable (VBNC) state was induced while more S. aureus entered this state than E. coli. Damaged bacterial outer structures were observed and the total concentrations of cellular protein and nucleic acid decreased for both bacteria after plasma treatment. The plasma-induced aqueous reactive species (RS) and intracellular ROS might produce detrimental effects to the bacteria, while S. aureus was less susceptible to the discharge after a 20-min exposure compared to E. coli.

[1]  P. Chu,et al.  Effects and Mechanism of Atmospheric-Pressure Dielectric Barrier Discharge Cold Plasma on Lactate Dehydrogenase (LDH) Enzyme , 2015, Scientific Reports.

[2]  J. Brisset,et al.  Peroxynitrite: A Re-examination of the Chemical Properties of Non-thermal Discharges Burning in Air Over Aqueous Solutions , 2012, Plasma Chemistry and Plasma Processing.

[3]  P. Lukeš,et al.  Membrane damage and active but nonculturable state in liquid cultures of Escherichia coli treated with an atmospheric pressure plasma jet. , 2015, Bioelectrochemistry.

[4]  D. Graves,et al.  Cold Atmospheric Plasma: Charged Species and Their Interactions With Cells and Tissues , 2008, IEEE Transactions on Plasma Science.

[5]  Martin Polak,et al.  Low temperature atmospheric pressure plasma sources for microbial decontamination , 2011 .

[6]  Selective effects of non-thermal atmospheric plasma on triple-negative breast normal and carcinoma cells through different cell signaling pathways , 2017, Scientific Reports.

[7]  G. Karp.  Cell and molecular biology : concepts and experiments / Gerald Karp , 1996 .

[8]  I. Wilson,et al.  Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. , 2000, European journal of biochemistry.

[9]  Radu Burlica,et al.  Formation of reactive species in gliding arc discharges with liquid water , 2006 .

[10]  Balaraman Kalyanaraman,et al.  Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. , 2012, Free radical biology & medicine.

[11]  B. Howard.  Clinical and Pathogenic Microbiology , 1987 .

[12]  M. M. Evans,et al.  Effect of atmospheric gas plasmas on cancer cell signaling , 2014, International journal of cancer.

[13]  Thomas von Woedtke,et al.  Estimation of Possible Mechanisms of Escherichia coli Inactivation by Plasma Treated Sodium Chloride Solution , 2011 .

[14]  Yuan Pan,et al.  An $RC$ Plasma Device for Sterilization of Root Canal of Teeth , 2009, IEEE Transactions on Plasma Science.

[15]  David B. Graves,et al.  Reactive species in non-equilibrium atmospheric-pressure plasmas: Generation, transport, and biological effects , 2016 .

[16]  Vladimír Scholtz,et al.  The Microbicidal Effect of Low‐Temperature Plasma Generated by Corona Discharge: Comparison of Various Microorganisms on an Agar Surface or in Aqueous Suspension , 2010 .

[17]  Petr Lukes,et al.  Formation of ROS and RNS in Water Electro-Sprayed through Transient Spark Discharge in Air and their Bactericidal Effects , 2013 .

[18]  A. Clyne,et al.  Hydroxyl Radical and Hydrogen Peroxide are Primarily Responsible for Dielectric Barrier Discharge Plasma-Induced Angiogenesis , 2011 .

[19]  M. Rong,et al.  Physicochemical processes in the indirect interaction between surface air plasma and deionized water , 2015 .

[20]  Xungai Wang,et al.  Efficient and Selectable Production of Reactive Species Using a Nanosecond Pulsed Discharge in Gas Bubbles in Liquid , 2016 .

[21]  Kostya Ostrikov,et al.  Inactivation of a 25.5 µm Enterococcus faecalis biofilm by a room-temperature, battery-operated, handheld air plasma jet , 2012 .

[22]  Giulio Jori,et al.  Photodynamic therapy in the treatment of microbial infections: Basic principles and perspective applications , 2006, Lasers in surgery and medicine.

[23]  L. Heller,et al.  Surface-dependent inactivation of model microorganisms with shielded sliding plasma discharges and applied air flow. , 2015, Bioelectrochemistry.

[24]  G. Moolenaar,et al.  Repair of UV damage in bacteria. , 2008, DNA repair.

[25]  J. Brisset,et al.  Combined Effects of Long-Living Chemical Species during Microbial Inactivation Using Atmospheric Plasma-Treated Water , 2010, Applied and Environmental Microbiology.

[26]  F. Scarano,et al.  Bactericidal efficacy of electrochemically activated solutions and of commercially available hypochlorite , 2010, British journal of biomedical science.

[27]  Ronny Brandenburg,et al.  The Role of Acidification for Antimicrobial Activity of Atmospheric Pressure Plasma in Liquids , 2010 .

[28]  C. Du,et al.  The Effects of Gas Composition on Active Species and Byproducts Formation in Gas–Water Gliding Arc Discharge , 2008 .

[29]  S. Fang,et al.  Sterilization of Bacillus subtilis Spores Using an Atmospheric Plasma Jet with Argon and Oxygen Mixture Gas , 2012 .

[30]  R. Thorn,et al.  The Effect of Long-Term Storage on the Physiochemical and Bactericidal Properties of Electrochemically Activated Solutions , 2012, International journal of molecular sciences.

[31]  Stephan Reuter,et al.  Plasmas for medicine , 2013 .

[32]  P. Chu,et al.  Atmospheric pressure plasma jet utilizing Ar and Ar/H2O mixtures and its applications to bacteria inactivation , 2014 .

[33]  Jing Fang,et al.  Reactive Oxygen Species in a Non-thermal Plasma Microjet and Water System: Generation, Conversion, and Contributions to Bacteria Inactivation—An Analysis by Electron Spin Resonance Spectroscopy† , 2012 .

[34]  S. Moreau,et al.  Low-temperature sterilization using gas plasmas: a review of the experiments and an analysis of the inactivation mechanisms. , 2001, International journal of pharmaceutics.

[35]  A. Pathak,et al.  Low‐temperature plasmas at atmospheric pressure: toward new pharmaceutical treatments in medicine , 2014, Fundamental & clinical pharmacology.

[36]  The Specific Vulnerabilities of Cancer Cells to the Cold Atmospheric Plasma-Stimulated Solutions , 2017, Scientific Reports.

[37]  G. Friedman,et al.  Inactivation of bacteria using dc corona discharge: role of ions and humidity , 2011, New journal of physics.

[38]  Z. Machala,et al.  Corona discharges with water electrospray for Escherichia coli biofilm eradication on a surface. , 2016, Bioelectrochemistry.

[39]  P. Chu,et al.  Cold atmospheric-pressure air plasma treatment of C6 glioma cells: Effects of reactive oxygen species in the medium produced by the plasma on cell death , 2017 .

[40]  Martin Clupek,et al.  Aqueous-phase chemistry and bactericidal effects from an air discharge plasma in contact with water: evidence for the formation of peroxynitrite through a pseudo-second-order post-discharge reaction of H2O2 and HNO2 , 2014 .

[41]  Gregor E. Morfill,et al.  The effect of low-temperature plasma on bacteria as observed by repeated AFM imaging , 2009 .

[42]  F. Huang,et al.  The disruption of bacterial membrane integrity through ROS generation induced by nanohybrids of silver and clay. , 2009, Biomaterials.

[43]  L. Heller,et al.  Antibacterial efficacy of a novel plasma reactor without an applied gas flow against methicillin resistant Staphylococcus aureus on diverse surfaces. , 2016, Bioelectrochemistry.

[44]  S. Hammerschmidt,et al.  Comparison of pulsed corona plasma and pulsed electric fields for the decontamination of water containing Legionella pneumophila as model organism. , 2016, Bioelectrochemistry.

[45]  Petr Lukes,et al.  Plasma chemistry and catalysis in gases and liquids , 2012 .

[46]  P. Chu,et al.  In vitro antimicrobial effects and mechanism of atmospheric-pressure He/O2 plasma jet on Staphylococcus aureus biofilm , 2017 .

[47]  Ming-hua Zhou,et al.  Formations of Active Species and By-Products in Water by Pulsed High-Voltage Discharge , 2007 .

[48]  Mounir Laroussi,et al.  Inactivation of bacteria by the plasma pencil , 2006 .

[49]  J. Trevors.  Viable but non-culturable (VBNC) bacteria: Gene expression in planktonic and biofilm cells. , 2011, Journal of microbiological methods.

[50]  장윤희,et al.  Y. , 2003, Industrial and Labor Relations Terms.

[51]  E. Cabiscol,et al.  Oxidative stress in bacteria and protein damage by reactive oxygen species. , 2000, International microbiology : the official journal of the Spanish Society for Microbiology.

[52]  David B. Graves,et al.  The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology , 2012 .

[53]  B Demple,et al.  Redox-operated genetic switches: the SoxR and OxyR transcription factors. , 2001, Trends in biotechnology.

[54]  F. Austin,et al.  Photodynamic therapy against common bacteria causing wound and skin infections. , 2012, Veterinary journal.

[55]  P. Bruggeman,et al.  Mechanisms of bacterial inactivation in the liquid phase induced by a remote RF cold atmospheric pressure plasma jet , 2013 .

[56]  H. Hirt,et al.  REACTIVE OXYGEN SPECIES: Metabolism, , 2004 .

[57]  Lenka Chladekova,et al.  Plasma agents in bio-decontamination by dc discharges in atmospheric air , 2010 .

[58]  P. Chu,et al.  Characteristics of DC Gas-Liquid Phase Atmospheric-Pressure Plasma and Bacteria Inactivation Mechanism , 2015 .

[59]  H. Hirt,et al.  Reactive oxygen species: metabolism, oxidative stress, and signal transduction. , 2004, Annual review of plant biology.

[60]  P. Chu,et al.  Observation of inactivation of Bacillus sbtilis spores under exposures of oxygen added argon atmospheric pressure plasma jet , 2014 .

[61]  Jue Zhang,et al.  Inactivation of Bacillus subtilis Spores in Water by a Direct‐Current, Cold Atmospheric‐Pressure Air Plasma Microjet , 2012 .

[62]  P. Chu,et al.  Bactericidal Effects of Plasma Induced Reactive Species in Dielectric Barrier Gas–Liquid Discharge , 2017, Plasma Chemistry and Plasma Processing.

[63]  P. Roslev,et al.  Formation of nonculturable Escherichia coli in drinking water , 2005, Journal of applied microbiology.

[64]  J. Brisset,et al.  Kinetics and Bacterial Inactivation Induced by Peroxynitrite in Electric Discharges in Air , 2012, Plasma Chemistry and Plasma Processing.

[65]  B. Benstaali,et al.  Acidity control of plasma-chemical oxidation: applications to dye removal, urban waste abatement and microbial inactivation , 2011 .

[66]  P. Lukeš,et al.  Generation of ozone by pulsed corona discharge over water surface in hybrid gas–liquid electrical discharge reactor , 2005 .

[67]  Zelong Zhang,et al.  Inactivation Effects of Non-Thermal Atmospheric-Pressure Helium Plasma Jet on Staphylococcus aureus Biofilms , 2015 .

[68]  David B. Graves,et al.  Long-term antibacterial efficacy of air plasma-activated water , 2011 .

[69]  Mounir Laroussi,et al.  Plasma interaction with microbes , 2003 .

[70]  A. Schindler,et al.  Destruction of oral biofilms formed in situ on machined titanium (Ti) surfaces by cold atmospheric plasma , 2013, Biofouling.

[71]  P. Chu,et al.  Genetic effects of an air discharge plasma on Staphylococcus aureus at the gene transcription level , 2015 .

[72]  M. Jünger,et al.  Antibacterial Activity of an Atmospheric Pressure Plasma Jet Against Relevant Wound Pathogens in vitro on a Simulated Wound Environment , 2010 .

[73]  O. Eichwald,et al.  Inactivation of Gram-positive biofilms by low-temperature plasma jet at atmospheric pressure , 2012 .

[74]  Satoshi Hamaguchi,et al.  Effects of pH on Bacterial Inactivation in Aqueous Solutions due to Low‐Temperature Atmospheric Pressure Plasma Application , 2010 .

[75]  O. Janoušková,et al.  The persistent microbicidal effect in water exposed to the corona discharge. , 2012, Physica medica : PM : an international journal devoted to the applications of physics to medicine and biology : official journal of the Italian Association of Biomedical Physics.