Skip to main content
SpringerLink
Log in

Kinetics and Bacterial Inactivation Induced by Peroxynitrite in Electric Discharges in Air

  • Original Paper
  • Published:
Plasma Chemistry and Plasma Processing Aims and scope Submit manuscript

Abstract

The mechanism of bacterial inactivation by electric discharges (non-thermal plasma) is examined on the basis of the action of the formed peroxynitrite and hydrogen peroxide on the external membrane of bacteria. A model accounts for the gas to liquid transfer of the active species which react with the bacterial wall at the liquid surface or /and in the bulk solution. Direct exposure to the glidarc discharge induces a pseudo zero order decay of the bacterial concentration, followed by a pseudo 1st order step for low concentrations. Post-discharge reactions develop after switching off the discharge according to a 1st order mechanism and show that active species drift in the solution. Additionally the bactericidal properties of pure water exposed to the discharge (i.e., “Plasma Activated Water”) was evidenced even 24 h after performing the plasma treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  1. Brisset J-L, Hnatiuc E (2012) Peroxynitrite: a re-examination of the chemical properties of non-thermal discharges burning in air over aqueous solutions. Plasma Chem Plasma Process. doi:10.1007/s11090-012-9384-x

  2. Brisset J-L, Moussa D, Doubla A, Hnatiuc E, Hnatiuc B, Kamgang Youbi G, Herry J-M, Naïtali N, Bellon-Fontaine M-N (2008) Chemical reactivity of discharges and temporal post-discharges in plasma treatment of aqueous media: examples of gliding discharges treated solutions. Ind Eng Chem Res 47:5761–5781

    Article  Google Scholar 

  3. Wang C, Deen W (2004) Peroxynitrite delivery methods for toxicity studies. Chem Res Toxicol 44:32–44

    Article  Google Scholar 

  4. Goldstein S, Squadrito G, Pryor W, Czapski G (1996) Direct and indirect oxidation mechanisms by peroxynitrite neither involving the hydroxyl radical. Free Radic Biol Med 21:966–974

    Article  Google Scholar 

  5. Koppenol W (1998) The basic chemistry of nitrogen monoxide and peroxynitrite. Free Radic Biol Med 25:385–391

    Article  Google Scholar 

  6. Goldstein S, Czapski G (1995) Direct and indirect oxidation mechanisms by peroxynitrite. Inorg Chem 34:4041–4048

    Article  Google Scholar 

  7. Oehmigen K, Hähnel M, Brandenburg R, Wilke Ch, Weltmann K-D, von Woedtke Th (2010) The role of acidification for antimicrobial activity of atmospheric pressure plasma in liquids. Plasma Process Polym 7:250–257

    Article  Google Scholar 

  8. Dobrynin D, Fridman G, Friedman G, Fridman A (2009) Physical and biological mechanism of direct plasma interaction with living tissue. New J Phys 11:115020

    Article  Google Scholar 

  9. Satoh K, MacGregor S, Anderson J, Woolsey G, Fouracre R (2007) Pulsed plasma disinfection of water containing E.coli. Jpn J Appl Phys 46:1137–1141

    Article  ADS  Google Scholar 

  10. McConnell P, Reasor M, Van Dyke K (2003) Three model systems measure oxidation /nitration damage caused by peroxynitrite. J Biosci 28:71–76

    Article  Google Scholar 

  11. Beckman J, Koppenol W (1996) Nitric oxide, superoxide and peroxynitrite: the good, the bad and the ugly. Am J Physiol Cell Physiol 271:C1424–C1437

    Google Scholar 

  12. Wu S, Wang L, Jocoby A, Jasinski K, Kubant R, Malinski T (2010) UV B light induced nitric oxide/peroxynitrite imbalance in keratinocytes-implication for apoptosis and necrosis. Photochem Photobiol 86:389–396

    Article  Google Scholar 

  13. Squadrito G, Pryor W (1998) Oxidative chemistry of nitric oxide: the roles of superoxide, peroxynitrite and carbon dioxide. Free Radic Biol Med 25:392–403

    Article  Google Scholar 

  14. Augusto O, Bonini M, Amanso A, Linares E, Santos C, De Menezes S (2002) Nitrogen dioxide and carbonate radical anion: two emerging radicals in biology. Free Radic Biol Med 32:841–859

    Article  Google Scholar 

  15. Zhang H, Squadrito G, Uppu R, Lemercier J-N, Cueto R, Pryor W (1997) Arch Biochem Biophys 339:183

    Article  Google Scholar 

  16. Uppu R, Squadrito G, Pryor W (1996) Arch Biochem Biophys 327:335

    Article  Google Scholar 

  17. Goldstein S, Czapski G (1998) J Am Chem Soc 120:3458

    Article  Google Scholar 

  18. Lu C, Lin J-M, Huie C, Yamada M (2004) Chimiluminescence study of carbonate and peroxynitrous acid and its application to the direct determination of nitrite bases on solid surface enhancement. Anal Chim Acta 510:29–34

    Article  Google Scholar 

  19. Butler A, Rutherford T, Short M, Ridd J (1997) Tyrosine nitration and peroxonitrite (peroxynitrite) isomerisation: 15N CIDNP NMR studies. J Chem Soc Chem Commun 669–670

  20. Radi R (2004) Nitric oxide, oxidants and protein tyrosine nitration. Proc Nat Acad Sci USA 106

  21. Radi R, Beckman J, Beckman T, Chen J, Marshall P, Freeman B (1991) Peroxynitrite oxidation of sulfhydrils. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem 266:4244–4250

    Google Scholar 

  22. Koppenol W, Moreno J, Pryor W, Ischiropoulos H, Beckman H (1992) Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem Res Toxicol 5:834–842

    Article  Google Scholar 

  23. Janka J, Kuzmin S, Maximov A, Titova J, Czernichowski A (1999) Investigation of the chemical action of the gliding and “point” arcs between the metallic electrode and aqueous solution. Plasma Chem Plasma Process 19:53–67

    Article  Google Scholar 

  24. Abdelmalek F, Gharbi S, Benstaali B, Addou A, Brisset J-L (2004) Plasmachemical degradation of azo dyes by humid air plasma : yellow supranol 4GL, scarlet red Nylosan F3GL and industrial wastes. Water Res 38:2339–2347

    Article  Google Scholar 

  25. Burlica R, Kirkpatrick M, Finney W, Clak R, Locke B (2004) Organic dye removal from aqueous solutions by glidarc discharges. J Electrostat 62:309–321

    Article  Google Scholar 

  26. Doubla A, Bouba Bello L, Fotso M, Brisset J-L (2007) Plasmachemical decolourization of bromothymol blue by gliding discharge. Dyes Pigment 77:118–124

    Article  Google Scholar 

  27. Moussa D, Doubla A, Kamgang Youbi G, Brisset J-L (2007) Post-discharge long life reactive intermediates involved in the plasmachemical degradation of azo dyes. IEEE Trans Plasma Sci 35:444–453

    Article  ADS  Google Scholar 

  28. Piroi D, Magureanu M, Mandache M, Parvulescu V (2008) Decomposition of methylene blue by a dielectric barrier discharge: optimization of the operating parameters. J Appl Phys 104:103306

    Article  ADS  Google Scholar 

  29. Brisset J-L, Benstaali B, Fanmoe J, Njoyim-Tamungang E (2011) Acidity control of the plasma-chemical treatments of organic wastes in aqueous effluents. Plasma Sour Sci Technol Special issue 20: 034021

  30. Doubla A, Tsagou-Sobze E, Moussa D, Burlica R, Hnatiuc E, Brisset JL (2007) Destruction plasmachimique d’urée et de thio-urée par décharge elctrique à pression atmospherique. Rev Sci Eau 20–3:265–272

    Google Scholar 

  31. Indarto A, Choi J, Lee H, Song H (2006) Treatment of CCl4 emission in a gliding arc plasma. Plasma Devices Oper 14:1–14

    Article  Google Scholar 

  32. Krawczyk K, Ulejczyk B (2003) Decommposition of chloromethanes in gliding discharges. Plasma Chem Plasma Process 23:265–281

    Article  Google Scholar 

  33. Estel L, Seguin D, Brisset J-L (1999) Plasma treatment of halogenated organic molecules. Ann N Y Acad Sci 891:199–206

    Article  ADS  Google Scholar 

  34. Ferenc Z, Wandrasz J (2004) Use of glidarc for decomposition of toluene vapours in hot exhausts. High Technol Plasma Process 8:31–37

    Google Scholar 

  35. Grossmanova H, Krcma F, Slanska K (2005) VOC destruction in atmospheric pressure plasma discharge. In: Proceedings of ISPC-17 (Toronto, Canada, 2005), pp 1216–1217

  36. Bartlett D, Church D, Bounds P, Koppenol W (1995) The kinetics of the oxidation of L-Ascorbic acid by peroxynitrite. Free Radic Biol Med 18:85–92

    Article  Google Scholar 

  37. Moussa D, Brisset J-L, Hnatiuc E, Decobert G (2006) Plasma chemical destruction of trilaurylamine from nuclear laboratories of reprocessing plants. Ind Eng Chem Res 45:23–29

    Article  Google Scholar 

  38. Pascal S, Moussa D, Hnatiuc E, Brisset J-L (2010) Plasma chemical degradation of phosphorous containing warfare agents stimulants. J Hazard Mater 175:1037–1041

    Article  Google Scholar 

  39. Sahni M, Locke B (2006) Degradation of chemical warfare agent simulant using gas-liquid pulsed streamer discharges. J Hazard Mater 137:1025–1034

    Article  Google Scholar 

  40. Moussa D, Brisset J-L (2003) Disposal of spent tributylphosphate by gliding arc plasma. J Hazard Mater 102:189–200

    Article  Google Scholar 

  41. Guezzar M, Abdelmalek F, Belhadj M, Benderdouche N, Addou A (2009) Enhancement of the bleaching and degradation of textile wastewaters by Glidarc discharge plasma in the presence of TiO2 catalyst. J Hazard Mater 164:1266–1274

    Article  Google Scholar 

  42. Guezzar M, Belhadj M, Abdelmalek F, Rais A, Addou A (2008) Non thermal plasma degradation of wastewater in presence of Titanium dioxide by gliding arc discharge. Int J Environ Waste Manage 2:458–470

    Article  Google Scholar 

  43. Doubla A, Laminsi S, Nzali S, Njoyim E, Kamsu-kom J, Brisset J-L (2007) Organic pollutant abatement and biodecontamination of brewery effluents by non-thermal plasma at atmospheric pressure. Chemosphere 69:332–337

    Article  Google Scholar 

  44. Gnokam Zumgang F, Doubla A, Brisset J-L (2010) Temporal post-discharge reactions in plasma chemical degradation of slaughterhouse effluents. Chem Eng Commun 98:483–493

    Article  Google Scholar 

  45. Njoyim E, Ghogomu P, Nzali S, Laminsi S, Doubla A, Brisset J-L (2009) Coupling Gliding discharge treatment and catalysis by oyster shell powder for pollution abatement of surface waters. Ind Eng Chem Res 48:9773–9780

    Article  Google Scholar 

  46. Trujillo M, Radi R (2002) Peroynitrite reaction with the reduced and the oxidized forms of lipoic acid: new insights into the reaction of peroxynitrite with thiols. Arch Biochem Biophys 397:91–98

    Article  Google Scholar 

  47. Vitrac H, Guespin J, Brisset J-L (2000) A microbiological investigation of the gliding arc treatment of aqueous media. In: Wagner H, Behnke J (eds) Proceedings of 7th international symposium high pressure low temperature plasma chemistry “Hakone-7” (Greifswald, Ge, 2000), vol 2, pp 393–397

  48. Burlica R, Grim R, Shih K, Balkwill D, Locke BR (2010) Bacterial inactivation using low gliding arc with water spray. Plasma Process Polym 7:640–649

    Article  Google Scholar 

  49. Maeda Y, Igura N, Shimoda M, Hayakawa I (2003) Bactericidal effect of atmospheric gas plasma on E. coli K12. Int Food Sci Technol 38:889–892

    Article  Google Scholar 

  50. Xingmin S, Yukang Y, Yanzhou S, Wang Y, Fengling P, Yuchang Q (2006) Experimental research of inactivation effect of low temperature plasma on bacteria. Plasma Sci Technol 8:569–572

    Article  Google Scholar 

  51. Choi J, Han I, Baik H, Lee M, Han D, Park J, Lee I, Song K, Lim Y (2006) Analysis of sterilization effect by pulsed DBD. J Electrostat 64:17–22

    Article  Google Scholar 

  52. Yu H, Perni S, Shi J, Wang D, Kong M, Sharma G (2006) Effects of cell surface loading and phase of growth in cold atmospheric gas plasma inactivation of E. coli K12. J Appl Microbiol 101:1323–1330

    Article  Google Scholar 

  53. Wang C, Wu Y, Li G (2008) Inactivation of E.coli with plasma generated by bipolar pulsed discharge in a 3 phase discharge plasma reactor. J Electrostat 66:71–78

    Article  Google Scholar 

  54. BenGadri R, Roth J, Montie T, Kelly-Wintenberg K, Tsai P, Helfritch D, Feldman P, Sherman D, Karakaya F, Chen Z (2000) Sterilization and plasma processing of room temperature surfaces with one atmosphere uniform glow discharge plasma (OAUGDP). Surf Coat Technol 131:528–542

    Article  Google Scholar 

  55. Laroussi M, Alexef I, Kang W (2000) Biological decontamination by nonthermal plasmas. IEEE Trans Plasma Sci 28:184–188

    Article  ADS  Google Scholar 

  56. Chen C, Lee H, Chang M (2009) Influence of pH on inactivation of aquatic microorganism with a gas -liquid pulsed electrical discharge. J Electrostat 67:703–708

    Article  Google Scholar 

  57. Chen C, Lee H, Chang M (2009) Ultrasound assisted plasma: a novel technique for inactivation of aquatic microorganisms. Environ Sci Technol 43:4493–4497

    Article  Google Scholar 

  58. Kamgang Youbi G, Herry J-M, Brisset J-L, Bellon-Fontaine M-N, Doubla A, Naïtali M (2008) Impact of disinfection efficiency of cell load and of planktonic/adherent/ detached state: case of Hafnia alvei inactivation by plasma activated water. Appl Microbiol Biotechnol 81:449–457

    Article  Google Scholar 

  59. Kamgang Youbi G, Herry J-M, Meylheuc T, Brisset J-L, Bellon-Fontaine M-N, Doubla A, Naitali M (20009) Microbial inactivation using a plasmachemical solution obtained by gliding electric discharges. Lett Appl Microbiol 49:13–18

  60. Naitali M, Hnatiuc B, Herry J-M, Bellon-Fontaine M-N, Brisset J-L (2009) Decontamination of chemical & microbial targets using electrical discharges. In: Brelles Marino G (ed) Biological and environmental applications of gas discharges plasmas, chap. 6. Nova Science Publ

  61. Naitali M, Kamgang Youbi G, Herry J-M, Bellon Fontaine M-N, Brisset J-L (2010) Combined effects of long life time chemical species during microbial inactivation by atmospheric plasma treated water. Appl Environ Microbiol 76:7662–7664

    Article  Google Scholar 

  62. Kamgang Youbi G, Herry J-M, Bellon-Fontaine M-N, Brisset J-L, Doubla A, Naitali M (2007) Evidence of temporal post-discharge decontamination of bacteria by gliding electric discharge. Application to Hafnia alvei. Appl Environ Microbiol 73:4791–4796

    Article  Google Scholar 

  63. Moreau M, Feuiloley M, Veron W, Meilheuc T, Chevalier S, Brisset J-L, Orange N (2007) Gliding arc discharge in the potato pathogen Erwinia carotovora atrospectica: Mechanism of lethal action and effects on membrane associated molecules. Appl Environ Microbiol 73:5904–5910

    Article  Google Scholar 

  64. Moreau M, Feuiloley M, Orange N, Brisset J-L (2005) Lethal effect of the gliding arc on Erwinia spp. J Appl Microbiol 98:1039–1046

    Article  Google Scholar 

  65. Kamgang Noubissi JO, Briandet R, Herry J-M, Brisset J-L, Naitali M (2007) Destruction of planktonic adherent and biofilms cells of St. Epidermidis using a gliding discharge in humid air. J Appl Microbiol 103:621–628

    Article  Google Scholar 

  66. Kamgang Noubissi JO, Naitali M, Herry J-M, Bellon-Fontaine M-N, Brisset J-L (2009) Increase in the hydrophilicity and Lewis acid-base properties on solid surfaces achieved by gliding discharge in humid air: effects on bacterial adherence. Plasma Sour Sci Technol 111:187–193

    ADS  Google Scholar 

  67. Laroussi M, Leipold F (2004) Evaluation of the role of reactive species heat and UV radiation in the inactivation of bacterial cells by air plasma at atmospheric pressure. Int J Mass Spectrom 233:81–86

    Article  Google Scholar 

  68. Kamgang Youbi G (2008) Propriétés réactives en post-decharge temporelle des décharges electriques glissantes dans l’air humide: Applications à la dégradation de colorants azoiques et à la decontamination microbienne (Reactivity of gliding discharges in temporal post-discharges conditions; applications to the degradation of azo dye and microbial decontamination). PhD dissertation (in French) University of Rouen (France)

  69. Boudam M, Moisan M, Saoudi B, Popovici C, Gherardi N, Massines F (2006) Bacterial spore inactivation by atmospheric pressure plasma in the presence or absence of UV photons as obtained with the same gas mixture. J Phys D Appl Phys 39:3494–3507

    Article  ADS  Google Scholar 

  70. Ma Y, Zhang G, Shi X, Xu G, Yang Y (2008) Chemical mechanisms of bacterial inactivation using DBD in atmospheric air. IEEE Trans Plasma Sci 36(4):1615–1620

    Article  ADS  Google Scholar 

  71. Kelly-Wintenberg K, Montie T, Brickman C, Roth J, Carr A, Sorge K, Wadsworth L, Tsai P (1998) Room Temperature sterilization of surfaces and fabrics with one atmosphere uniform glow discharge plasma. J Ind Microbiol Biotechnol 20:69–74

    Article  Google Scholar 

  72. Ekem N, Akan T, Akgun Y, Kiremitci A, Pat S, Musa G (2006) Sterilization of St aureus by atmospheric pressure pulsed plasma. Surf Coat Technol 201:993–997

    Article  Google Scholar 

  73. Akitsu T, Ohkawa H, Tsuji M, Kimura H, Kogoma M (2005) Plasma sterilization using glow discharge at atmospheric pressure. Surf Coat Technol 193:29–34

    Article  Google Scholar 

  74. Roustan M, Mallevialle J, Roques H, Jones J (1981) Mass transfer of Ozone to water: a fundamental study. Ozone Sci Eng 2:337–344

    Article  Google Scholar 

Download references

Author information

Author notes

  1. Georges Kamgang

    Present address: Laboratory of Mineral Chemistry, Faculty of Sciences, University of Yaounde I, POB 8205, Yaounde, Cameroon

Authors and Affiliations

  1. Institut Micalis, AgroParisTech UMR-732(BMH), 25 Av. de la République, 91744, Massy, France

    Murielle Naïtali, Jean-Marie Herry & Georges Kamgang

  2. Universitate Apollonia din Iasi, str. Pacurari Nr11, 700511, Iasi, Romania

    Eugen Hnatiuc

  3. Chemistry Department, Faculty of Sciences, University of Rouen, 76821, Mont-Saint Aignan, France

    Georges Kamgang & Jean-Louis Brisset

Authors
  1. Murielle Naïtali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean-Marie Herry
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eugen Hnatiuc
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Georges Kamgang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jean-Louis Brisset
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean-Louis Brisset.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Naïtali, M., Herry, JM., Hnatiuc, E. et al. Kinetics and Bacterial Inactivation Induced by Peroxynitrite in Electric Discharges in Air. Plasma Chem Plasma Process 32, 675–692 (2012). https://doi.org/10.1007/s11090-012-9383-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11090-012-9383-y

Keywords

Search

Navigation