Inactivation of microbes and macromolecules by atmospheric-pressure plasma jets

Plasma is ionized gas, which is found in various forms in nature and can also be generated artificially. A variety of cold atmospheric-pressure plasmas are currently being investigated for their clinical utility, and first studies reporting on the treatment of patients showed that plasma treatment may support the wound healing process. One of the benefits of plasma treatment is the effective inactivation of bacteria including tenacious pathogens such as Pseudomonas aeruginosa or multiresistant Staphylococcus aureus (MRSA). Neither the molecular mechanisms promoting wound healing nor those underlying bacterial inactivation are fully understood yet. The review has a focus on plasma jets, a particular type of cold atmospheric-pressure plasma sources featuring an indirect treatment whereby the treated substrates do not come into contact with the plasma directly but are exposed to the plasma-emitted reactive species and photons. Such plasma jets are being employed as tools in basic research regarding the effects of plasmas on biological samples. This review provides a brief overview on the recent clinical investigations into the benefits of cold atmospheric-pressure plasmas. It then describes our current understanding of the mechanisms leading to bacterial inactivation and inactivation of biomacromolecules gained by employing plasma jets.

[1]  Joachim Dissemond,et al.  Influence of pH on wound-healing: a new perspective for wound-therapy? , 2007, Archives of Dermatological Research.

[2]  Karl H. Schoenbach,et al.  Non-Equilibrium Air Plasmas at Atmospheric Pressure , 2004 .

[3]  W. Stolz,et al.  Cold Atmospheric Air Plasma Sterilization against Spores and Other Microorganisms of Clinical Interest , 2012, Applied and Environmental Microbiology.

[4]  A. Lichtenberg,et al.  Principles of Plasma Discharges and Materials Processing , 1994 .

[5]  G. Georghiou,et al.  Bactericidal Action of the Reactive Species Produced by Gas-Discharge Nonthermal Plasma at Atmospheric Pressure: A Review , 2006, IEEE Transactions on Plasma Science.

[6]  L. Deelman,et al.  Delayed Effects of Cold Atmospheric Plasma on Vascular Cells , 2008 .

[7]  R. Gesche,et al.  Biological effects of nitric oxide generated by an atmospheric pressure gas-plasma on human skin cells. , 2011, Nitric oxide : biology and chemistry.

[8]  Akira Mizuno,et al.  Biological Evaluation of DNA Damage in Bacteriophages Inactivated by Atmospheric Pressure Cold Plasma , 2010 .

[9]  R. Leask,et al.  Effects of Non‐thermal Plasmas on DNA and Mammalian Cells , 2010 .

[10]  Michael Landthaler,et al.  Plasma medicine: possible applications in dermatology , 2010, Journal der Deutschen Dermatologischen Gesellschaft = Journal of the German Society of Dermatology : JDDG.

[11]  Ahmed Khacef,et al.  Application of atmospheric non thermal plasma-catalysis hybrid system for air pollution control: Toluene removal , 2011 .

[12]  J. Lackmann,et al.  The Role of VUV Radiation in the Inactivation of Bacteria with an Atmospheric Pressure Plasma Jet , 2011, 1105.6260.

[13]  Chong Zhang,et al.  Rapid Mutation of Spirulina platensis by a New Mutagenesis System of Atmospheric and Room Temperature Plasmas (ARTP) and Generation of a Mutant Library with Diverse Phenotypes , 2013, PloS one.

[14]  A. Pruden,et al.  Differential gene expression in Escherichia coli following exposure to nonthermal atmospheric pressure plasma , 2009, Journal of applied microbiology.

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

[16]  Bruce R. Locke,et al.  Review of the methods to form hydrogen peroxide in electrical discharge plasma with liquid water , 2011 .

[17]  J. Schuette,et al.  The acidification of lipid film surfaces by non-thermal DBD at atmospheric pressure in air , 2009 .

[18]  Lewi Tonks,et al.  OSCILLATIONS IN IONIZED GASES , 1961 .

[19]  K. Weltmann,et al.  Quantitative detection of plasma-generated radicals in liquids by electron paramagnetic resonance spectroscopy , 2013 .

[20]  E. Stoffels,et al.  Reattachment and Apoptosis After Plasma-Needle Treatment of Cultured Cells , 2006, IEEE Transactions on Plasma Science.

[21]  Gregory Fridman,et al.  Floating Electrode Dielectric Barrier Discharge Plasma in Air Promoting Apoptotic Behavior in Melanoma Skin Cancer Cell Lines , 2007 .

[22]  X. Xing,et al.  Novel mutation breeding method for Streptomyces avermitilis using an atmospheric pressure glow discharge plasma , 2010, Journal of applied microbiology.

[23]  Gregor E. Morfill,et al.  Cold Atmospheric Plasma (CAP) Changes Gene Expression of Key Molecules of the Wound Healing Machinery and Improves Wound Healing In Vitro and In Vivo , 2013, PloS one.

[24]  M Landthaler,et al.  Successful and safe use of 2 min cold atmospheric argon plasma in chronic wounds: results of a randomized controlled trial , 2012, The British journal of dermatology.

[25]  E. Takai,et al.  Protein Inactivation by Low‐temperature Atmospheric Pressure Plasma in Aqueous Solution , 2012 .

[26]  A. Kramer,et al.  Human Mononuclear Cell Survival and Proliferation is Modulated by Cold Atmospheric Plasma Jet , 2013 .

[27]  L. Prakash.  Molecular and environmental aspects of mutagenesis , 1974 .

[28]  Alisa Morss Clyne,et al.  Non-thermal dielectric barrier discharge plasma induces angiogenesis through reactive oxygen species , 2012, Journal of The Royal Society Interface.

[29]  M. Schön,et al.  Atmospheric pressure plasma in dermatology: Ulcus treatment and much more , 2013 .

[30]  R. Wolf.  Atmospheric Pressure Plasma for Surface Modification: Wolf/Atmospheric , 2012 .

[31]  DNA damage in mammalian cells by non-thermal atmospheric pressure microsecond pulsed dielectric barrier discharge plasma is not mediated by ozone , 2010, ICOPS 2010.

[32]  Z. Li,et al.  SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA. , 1994, The Journal of biological chemistry.

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

[34]  Kevin Davis,et al.  Reactive nitrogen species produced in water by non-equilibrium plasma increase plant growth rate and nutritional yield , 2013 .

[35]  S. McMahon,et al.  Cold atmospheric pressure plasma jet interactions with plasmid DNA , 2011 .

[36]  G Daeschlein,et al.  Alleviation of chronic venous leg ulcers with a hand‐held dielectric barrier discharge plasma generator (PlasmaDerm® VU‐2010): results of a monocentric, two‐armed, open, prospective, randomized and controlled trial (NCT01415622) , 2015, Journal of the European Academy of Dermatology and Venereology : JEADV.

[37]  James L. Walsh,et al.  Probing bactericidal mechanisms induced by cold atmospheric plasmas with Escherichia coli mutants , 2007 .

[38]  Oliver Höfft,et al.  Electron spectroscopic analysis of the human lipid skin barrier: cold atmospheric plasma‐induced changes in lipid composition , 2012, Experimental dermatology.

[39]  J. Lackmann,et al.  Separation of VUV/UV photons and reactive particles in the effluent of a He/O2 atmospheric pressure plasma jet , 2011, 1105.2207.

[40]  J. Lackmann,et al.  Characterization of Damage to Bacteria and Bio-macromolecules Caused by (V)UV Radiation and Particles Generated by a Microscale Atmospheric Pressure Plasma Jet , 2012 .

[41]  Kwon-Yong Lee,et al.  Sterilization of Escherichia coli and MRSA using microwave-induced argon plasma at atmospheric pressure , 2005 .

[42]  G. Shama,et al.  Cold atmospheric plasma decontamination of the pericarps of fruit. , 2008, Journal of food protection.

[43]  M. Hecker,et al.  Characterization of the global impact of low temperature gas plasma on vegetative microorganisms , 2011, Proteomics.

[44]  A. Kramer,et al.  Tissue Tolerable Plasma (TTP) induces apoptosis in pancreatic cancer cells in vitro and in vivo , 2012, BMC Cancer.

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

[46]  Michael G. Kong,et al.  Protein destruction by atmospheric pressure glow discharges , 2007 .

[47]  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 .

[48]  Wilhelm Stolz,et al.  Cold atmospheric plasma: a successful treatment of lesions in Hailey-Hailey disease. , 2011, Archives of dermatology.

[49]  E. Sage,et al.  DNA Oxidation by Reactive Oxygen Species Produced by Atmospheric Pressure Microplasmas , 2012 .

[50]  Steffen Brinckmann,et al.  Photons and particles emitted from cold atmospheric-pressure plasma inactivate bacteria and biomolecules independently and synergistically , 2013, Journal of The Royal Society Interface.

[51]  J. Zimmermann,et al.  Contact-free cold atmospheric plasma treatment of Deinococcus radiodurans , 2012, Journal of Industrial Microbiology & Biotechnology.

[52]  A. Lichtenberg,et al.  Principles of Plasma Discharges and Materials Processing: Lieberman/Plasma 2e , 2005 .

[53]  Michael G. Kong,et al.  Protein destruction by a helium atmospheric pressure glow discharge: Capability and mechanisms , 2007 .

[54]  Jianjun Shi,et al.  Physical Mechanisms of Inactivation of Bacillus subtilis Spores Using Cold Atmospheric Plasmas , 2006, IEEE Transactions on Plasma Science.

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

[56]  A. Clyne,et al.  Cell proliferation following non-thermal plasma is related to reactive oxygen species induced fibroblast growth factor-2 release , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[57]  R. Brandenburg,et al.  Plasma-Liquid Interactions: Chemistry and Antimicrobial Effects , 2012 .

[58]  Sean P. Gorman,et al.  Eradication of Pseudomonas aeruginosa Biofilms by Atmospheric Pressure Non-Thermal Plasma , 2012, PloS one.

[59]  Y. Akishev,et al.  Plasma for Bio-Decontamination, Medicine and Food Security , 2012, NATO Science for Peace and Security Series A: Chemistry and Biology.

[60]  Gregor E. Morfill,et al.  Plasma medicine: an introductory review , 2009 .

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

[62]  Inactivation property of microorganisms in water irradiated by atmospheric‐pressure plasma using dielectric barrier discharge , 2013 .

[63]  Michel Moisan,et al.  Decontamination of Prions by the Flowing Afterglow of a Reduced-pressure N2O2 Cold-plasma , 2012 .

[64]  N. Bibinov,et al.  Electrical and spectroscopic characterization of a surgical argon plasma discharge , 2013 .

[65]  Mounir Laroussi,et al.  Evaluation of the roles of reactive species, heat, and UV radiation in the inactivation of bacterial cells by air plasmas at atmospheric pressure , 2004 .

[66]  M. Radman,et al.  Phenomenology of an inducible mutagenic DNA repair pathway in Escherichia coli: SOS repair hypothesis , 1974 .

[67]  Adriana Laca,et al.  Cold atmospheric gas plasma disinfection of chicken meat and chicken skin contaminated with Listeria innocua. , 2011, Food microbiology.

[68]  A. le Pape,et al.  Effects of a Non Thermal Plasma Treatment Alone or in Combination with Gemcitabine in a MIA PaCa2-luc Orthotopic Pancreatic Carcinoma Model , 2012, PloS one.

[69]  Sophie Lerouge,et al.  Plasma Sterilization: A Review of Parameters, Mechanisms, and Limitations , 2001 .

[70]  Oliver Franken,et al.  Reduction of Bacillus Subtilis and Aspergillus Niger spores using nonthermal atmospheric gas discharges , 2002 .

[71]  Laurent Catoire,et al.  Plasma thermal conversion of bio‐oil for hydrogen production , 2012 .

[72]  J. Bernhardt,et al.  Common versus noble Bacillus subtilis differentially responds to air and argon gas plasma , 2013, Proteomics.

[73]  Mounir Laroussi,et al.  Low Temperature Plasma-Based Sterilization: Overview and State-of-the-Art , 2005 .

[74]  B Demple,et al.  Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[75]  R. Sensenig,et al.  Live Pig Skin Tissue and Wound Toxicity of Cold Plasma Treatment , 2011 .

[76]  J Francis,et al.  Biological effects , 1980, Advanced Series on Ocean Engineering.

[77]  C. Kieda,et al.  ROS implication in a new antitumor strategy based on non‐thermal plasma , 2012, International journal of cancer.

[78]  A. Fridman,et al.  Effects of Non-Thermal Plasma on Mammalian Cells , 2011, PloS one.

[79]  N. Mason,et al.  DNA strand scission induced by a non-thermal atmospheric pressure plasma jet. , 2010, Physical chemistry chemical physics : PCCP.