Cited by 51Plasma Applications and DiagnosticsMicrobial Inactivation MethodsPhotodynamic Therapy Research Studies

Direct and Indirect Bactericidal Effects of Cold Atmospheric-Pressure Microplasma and Plasma Jet

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Yahaya, Ahmad Guji, Okuyama, Tomohiro, Kristof, Jaroslav, Blajan, Marius Gabriel, Shimizu, Kazuo·2021·Molecules

Abstract

The direct and indirect bactericidal effects of dielectric barrier discharge (DBD) cold atmospheric-pressure microplasma in an air and plasma jet generated in an argon-oxygen gas mixture was investigated on Staphylococcus aureus and Cutibacterium acnes. An AC power supply was used to generate plasma at relatively low discharge voltages (0.9–2.4 kV) and frequency (27–30 kHz). Cultured bacteria were cultivated at a serial dilution of 10−5, then exposed to direct microplasma treatment and indirect treatment through plasma-activated water (PAW). The obtained results revealed that these methods of bacterial inactivation showed a 2 and 1 log reduction in the number of survived CFU/mL with direct treatment being the most effective means of treatment at just 3 min using air. UV–Vis spectroscopy confirmed that an increase in treatment time at 1.2% O2, 98.8% Ar caused a decrease in O2 concentration in the water as well as a decrease in absorbance of the peaks at 210 nm, which are attributed NO2− and NO3− concentration in the water, termed denitratification and denitritification in the treated water, respectively.

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  • The antimicrobial effects of CP, involving reactive species attacking bacterial cells, damaging cell walls, increasing membrane permeability, leading to cell membrane rupture, damage to organelles, proteins, and nucleic acids, and microbial cell death, may explain the shifts in genera.

    “The underlying mechanism for these shifts may involve the antimicrobial effects of CP: reactive species generated during CP treatment can attack bacterial cells, damaging cell walls to increase membrane permeability. This process ultimately leads to cell membrane rupture, followed by damage to organelles, proteins, and nucleic acids, culminating in microbial cell death [55,56].”

    From Effect of Atmospheric Cold Plasma Treatment on the Microorganism Growth, Diversity, and Quality of Coconut Water During Refrigerator Storage (2025) · cites this paper as [56]

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  1. [1]Klämpfl T.G. Isbary G. Shimizu T. Li Y.-F. Zimmermann J.L. Stolz W. Schlegel J. Morfill G.E. Schmidt H.-U. Cold Atmospheric Air Plasma Sterilization against Spores and Other Microorganisms of Clinical Interest Appl. Environ. Microbiol. 2012 78 5077 5082 10.1128/AEM.00583-12 22582068 PMC3416436 · DOI
  2. [2]Athanasiou K. Sterilization, toxicity, biocompatibility and clinical applications of polylactic acid/ polyglycolic acid copolymers Biomaterials 1996 17 93 102 10.1016/0142-9612(96)85754-1 8624401 · DOI · Paper page
  3. [3]Lerouge S. Tabrizian M. Wertheimer M.R. Marchand R. Yahia L. Safety of plasma-based sterilization: Surface modifications of polymeric medical devices induced by Sterrad and Plazlyte processes Biol. Med. Mater. Eng. 2002 12 3 13 11847405
  4. [4]E Holy C. Cheng C. E Davies J. Shoichet M.S. Optimizing the sterilization of PLGA scaffolds for use in tissue engineering Biomaterials 2000 22 25 31 10.1016/S0142-9612(00)00136-8 11085380 · DOI
  5. [5]Matthews I.P. Gibson C. Samuel A.H. Sterilisation of implantable devices Clin. Mater. 1994 15 191 215 10.1016/0267-6605(94)90082-5 10172076 · DOI
  6. [6]Laroussi M. Sterilization of contaminated matter with an atmospheric pressure plasma IEEE Trans. Plasma Sci. 1996 24 1188 1191 10.1109/27.533129 · DOI
  7. [7]Kayes M.M. Critzer F.J. Kelly-Wintenberg K. Roth J.R. Montie T.C. Golden D.A. Inactivation of Foodborne Pathogens Using A One Atmosphere Uniform Glow Discharge Plasma Foodborne Pathog. Dis. 2007 4 50 59 10.1089/fpd.2006.62 17378708 · DOI
  8. [8]Ehlbeck J. Schnabel U. Von Woedtke T. Brandenburg R. Weltmann K.D. Polak M. Winter J. Von dem Hagen T. Low temperature atmospheric pressure plasma sources for microbial decontamination J. Appl. Phys. 2011 44 18 10.1088/0022-3727/44/1/013002 · DOI
  9. [9]Kong M.G. Kroesen G. Morfill G. Nosenko T. Shimizu T. Van Dijk J. Zimmermann J.L. Plasma medicine: An introductory review New J. Phys. 2009 11 115012 10.1088/1367-2630/11/11/115012 · DOI
  10. [10]Laroussi M. Low Temperature Plasma-Based Sterilization: Overview and State-of-the-Art Plasma Process. Polym. 2005 2 391 400 10.1002/ppap.200400078 · DOI
  11. [11]Stoffels E. Sakiyama Y. Graves D.B. Cold Atmospheric Plasma: Charged Species and Their Interactions with Cells and Tissues IEEE Trans. Plasma Sci. 2008 36 1441 1457 10.1109/TPS.2008.2001084 · DOI
  12. [12]Yahaya A.G. Tomomichi A. Mustafa F. Jaroslav K. Blajan M. Shimizu K. Skin treatment: Sterilization and Drug Delivery by Microplasma Proceedings of the 6th Internarional Symposium toward the Future of Advanced Researches in Shizuoka University 2020(ISFAR-SU2020) Hamamatsu, Japan 5 March 2020 54
  13. [13]Suschek C.V. Opländer C. The application of cold atmospheric plasma in medicine: The potential role of nitric oxide in plasma-induced effects Clin. Plasma Med. 2016 4 10.1016/j.cpme.2016.05.001 · DOI
  14. [14]Park S. Choe W. Moon S.Y. Yoo S.J. Electron characterization in weakly ionized collisional plasmas: From principles to techniques Adv. Phys. X 2018 4 10.1080/23746149.2018.1526114 · DOI
  15. [15]Kolb J.F. Mohamed A.-A.H. Price R.O. Swanson R.J. Bowman A. Chiavarini R.L. Stacey M. Schoenbach K.H. Cold atmospheric pressure air plasma jet for medical applications Appl. Phys. Lett. 2008 92 241501 10.1063/1.2940325 · DOI
  16. [16]Lu X. Wu S. Gou J. Pan Y. An atmospheric-pressure, high-aspect-ratio, cold micro-plasma Sci. Rep. 2014 4 7488 10.1038/srep07488 25502006 PMC4265786 · DOI
  17. [17]Recek N. Andjelic S. Hojnik N. Filipič G. Lazović S. Vesel A. Primc G. Mozetič M. Hawlina M. Petrovski G. Microplasma Induced Cell Morphological Changes and Apoptosis of Ex Vivo Cultured Human Anterior Lens Epithelial Cells—Relevance to Capsular Opacification PLoS ONE 2016 11 e0165883 10.1371/journal.pone.0165883 27832099 PMC5104483 · DOI
  18. [18]Takahashi R. Shimizu K. Numabe Y. Effects of microplasma irradiation on human gingival fibroblasts Odontology 2015 103 194 202 10.1007/s10266-014-0157-2 24916282 · DOI
  19. [19]Shimizu K. A Tran N. Hayashida K. Blajan M. Comparison of atmospheric microplasma and plasma jet irradiation for increasing of skin permeability J. Phys. D Appl. Phys. 2016 49 315201 10.1088/0022-3727/49/31/315201 · DOI
  20. [20]Pai K. Timmons C. Roehm K.D. Ngo A. Narayanan S.S. Ramachandran A. Jacob J.D. Ma L.M. Madihally S.V. Investigation of the Roles of Plasma Species Generated by Surface Dielectric Barrier Discharge Sci. Rep. 2018 8 1 13 10.1038/s41598-018-35166-0 30420780 PMC6232176 · DOI
  21. [21]Nicol M.J. Brubaker T.R. Ii B.J.H. Simmons A.N. Kazemi A. Geissel M.A. Whalen C.T. Siedlecki C.A. Bilén S.G. Knecht S.D. Antibacterial effects of low-temperature plasma generated by atmospheric-pressure plasma jet are mediated by reactive oxygen species Sci. Rep. 2020 10 1 11 10.1038/s41598-020-59652-6 32080228 PMC7033188 · DOI
  22. [22]Shimizu K. Blajan M. Tatematsu S. Basic Study of Remote Disinfection and Sterilization Effect by Using Atmospheric Microplasma IEEE Trans. Ind. Appl. 2012 48 1182 1188 10.1109/TIA.2012.2199953 · DOI
  23. [23]Shimizu K. Komuro Y. Tatematsu S. Blajan M. Study of Sterilization and Disinfection in Room Air by Using Atmospheric Microplasma Pharm. Anal. Acta 2011 S1 10.4172/2153-2435.S1-001 · DOI
  24. [24]Mitra S. Nguyen L.N. Akter M. Park G. Choi E.H. Kaushik N.K. Impact of ROS Generated by Chemical, Physical, and Plasma Techniques on Cancer Attenuation Cancers 2019 11 1030 10.3390/cancers11071030 PMC6678366 31336648 · DOI
  25. [25]Fridman A. Plasma Chemistry Cambridge University Press Cambridge, UK 2012
  26. [26]Kim S.J. Chung T.H. Cold atmospheric plasma jet-generated RONS and their selective effects on normal and carcinoma cells Sci. Rep. 2016 6 20332 10.1038/srep20332 26838306 PMC4738260 · DOI
  27. [27]Bogaerts A. Yusupov M. Razzokov J. Van der Paal J. Plasma for cancer treatment: How can RONS penetrate through the cell membrane? Answers from computer modeling Front. Chem. Sci. 2019 13 253 263 10.1007/s11705-018-1786-8 · DOI
  28. [28]Hwang I. Jeong J. You T. Jung J. Water electrode plasma discharge to enhance the bacterial inactivation in water Biotechnol. Biotechnol. Equip. 2018 32 530 534 10.1080/13102818.2017.1321969 · DOI
  29. [29]De Backer J. Razzokov J. Hammerschmid D. Mensch C. Hafideddine Z. Kumar N. Van Raemdonck G. Yusupov M. Van Doorslaer S. Johannessen C. The effect of reactive oxygen and nitrogen species on the structure of cytoglobin: A potential tumor suppressor Redox Biol. 2018 19 1 10 10.1016/j.redox.2018.07.019 30081385 PMC6084017 · DOI
  30. [30]Oehmigen K. Hähnel M. Brandenburg R. Wilke C. Weltmann K.-D. Von Woedtke T. The Role of Acidification for Antimicrobial Activity of Atmospheric Pressure Plasma in Liquids Plasma Process. Polym. 2010 7 250 257 10.1002/ppap.200900077 · DOI
  31. [31]Kaushik N.K. Ghimire B. Li Y. Adhikari M. Veerana M. Kaushik N. Jha N. Adhikari B. Lee S.-J. Masur K. Biological and medical applications of plasma-activated media, water and solutions Biol. Chem. 2018 400 39 62 10.1515/hsz-2018-0226 30044757 · DOI
  32. [32]Yun S. Yoon S.-Y. Hong E.J. Giri S.S. Kim S.G. Han S.J. Kwon J. Oh W.T. Bin Lee S. Park S.C. Effect of plasma-activated water, used as a disinfectant, on the hatch rate of dormant cysts of the Artemia salina Aquaculture 2020 523 735232 10.1016/j.aquaculture.2020.735232 · DOI
  33. [33]Lerouge S. Wertheimer M.R. Yahia L. Plasma Sterilization: A Review of Parameters, Mechanisms, and Limitations Plasmas Polym. 2001 6 175 188 10.1023/A:1013196629791 · DOI
  34. [34]Lowy F.D. Staphylococcus aureusInfections N. Engl. J. Med. 1998 339 520 532 10.1056/NEJM199808203390806 9709046 · DOI
  35. [35]Centers for Disease Control and Prevention (CDC) Outbreaks of community-associated methicillin-resistant Staphylococcus aureus skin infections—Los Angeles County, California, 2002-2003 MMWR Morb. Mortal Wkly. Rep. 2003 52 88 12588006
  36. [36]Boucher H.W. Corey G.R. Epidemiology of Methicillin-ResistantStaphylococcus aureus Clin. Infect. Dis. 2008 46 S344 S349 10.1086/533590 18462089 · DOI
  37. [37]Patel A. Calfee R.P. Plante M. Fischer S.A. Green A. Propionibacterium acnes colonization of the human shoulder J. Shoulder Elb. Surg. 2009 18 897 902 10.1016/j.jse.2009.01.023 19362854 · DOI
  38. [38]Levy P.Y. Fenollar F. Stein A. Borrione F. Cohen E. LeBail B. Raoult D. Propionibacterium acnesPostoperative Shoulder Arthritis: An Emerging Clinical Entity Clin. Infect. Dis. 2008 46 1884 1886 10.1086/588477 18462110 · DOI
  39. [39]Frangiamore S.J. Saleh A. Grosso M.J. Alolabi B. Bauer T.W. Iannotti J.P. Ricchetti E.T. Early Versus Late Culture Growth of Propionibacterium acnes in Revision Shoulder Arthroplasty J. Bone Jt. Surg. Am. Vol. 2015 97 1149 1158 10.2106/JBJS.N.00881 26178890 · DOI
  40. [40]Del Greco F.P. Kaufman F. Lifetime and reactions of OH radicals in discharge-flow systems Discuss. Faraday Soc. 1962 33 128 138 10.1039/df9623300128 · DOI
  41. [41]Szili E.J. Oh J.-S. Hong S.-H. Hatta A. Short R.D. Probing the transport of plasma-generated RONS in an agarose target as surrogate for real tissue: Dependency on time, distance and material composition J. Phys. D Appl. Phys. 2015 48 202001 10.1088/0022-3727/48/20/202001 · DOI
  42. [42]Oh J.-S. Szili E.J. Hatta A. Ito M. Shirafuji T. Oh I. Ito Tailoring the Chemistry of Plasma-Activated Water Using a DC-Pulse-Driven Non-Thermal Atmospheric-Pressure Helium Plasma Jet Plasma 2019 2 10 10.3390/plasma2020010 · DOI
  43. [43]Oh J.-S. Szili E.J. Gaur N. Hong S.-H. Furuta H. Short R.D. Hatta A. In-situ UV Absorption Spectroscopy for Monitoring Transport of Plasma Reactive Species through Agarose as Surrogate for Tissue J. Photopolym. Sci. Technol. 2015 28 439 444 10.2494/photopolymer.28.439 · DOI
  44. [44]Gómez M. Effect of dissolved oxygen concentration on nitrate removal from groundwater using a denitrifying submerged filter J. Hazard. Mater. 2002 90 267 278 10.1016/S0304-3894(01)00353-3 11893425 · DOI
  45. [45]Nakajima M. Hayamizu T. Nishimura H. Effect of oxygen concentration on the rates of denitratification and denitrification in the sediments of an eutrophic lake Water Res. 1984 18 335 338 10.1016/0043-1354(84)90108-8 · DOI
  46. [46]Schroeder J. Croot P. Von Dewitz B. Waller U. Hanel R. Potential and limitations of ozone for the removal of ammonia, nitrite, and yellow substances in marine recirculating aquaculture systems Aquac. Eng. 2011 45 35 41 10.1016/j.aquaeng.2011.06.001 · DOI
  47. [47]Rahmadi P. Kim Y.R. Effects of different levels of ozone on ammonia, nitrite, nitrate, and dissolved organic carbon in sterilization of seawater Desalin. Water Treat. 2013 52 4413 4422 10.1080/19443994.2013.803702 · DOI

Cited by

Authors
Yahaya, A. G., Okuyama, T., Kristof, J., Blajan, M. G., & Shimizu, K.
Affiliations
  • Shizuoka University (JP)
  • Organization for Innovation and Social Collaboration, Shizuoka University, Hamamatsu 432-8561, Japan
Corresponding author
Yahaya, Ahmad Guji
Venue
Molecules
Publisher
MDPI AG
Published
2021-04-26
Volume
26
Issue
9
Pages
2523
ISSN
1420-3049 (ISSN-L)
OpenAlex
W3159121559
Cited by
51
References
0
Citations by year
2026: 3 · 2025: 18 · 2024: 10 · 2023: 9 · 2022: 10 · 2021: 1
FWCI
3.96
Type
journal article
Language
en
Open access
Locations
  • Molecules (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Shizuoka University
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Plasma Applications and Diagnostics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Photodynamic Therapy Research Studies
Keywords
plasma jet, dielectric barrier discharge, bactericidal activity, Staphylococcus aureus, Propionibacterium acnes, plasma-activated water, argon-oxygen mixtures, nitrate reduction, nitrite reduction
MeSH terms
Anti-Bacterial Agents, Atmospheric Pressure, Microbial Sensitivity Tests, Ozone, Staphylococcus aureus, Sterilization, Water, Reactive Oxygen Species, Reactive Nitrogen Species, Plasma Gases

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