Abstract
An atmospheric helium dielectric barrier discharge is used to treat Staphylococcus aureus (S. aureus) to study plasma bacteria inactivation in the gas–liquid phase. Optical emission spectroscopy, mass spectrometry, and spectrophotometry are used to analyze the products induced by the plasma in the liquid as well as interactions between the liquid products and bacteria. The bactericidal mechanisms associated with the liquid products and different treatment protocols are investigated. The short-lived reactive species produce efficient inactivation effects in the direct plasma treatment and long-lived reactive species show continuous residual bactericidal effects. Additionally, even the minor initial damage caused by direct plasma exposure promotes the residual inactivation effect. After the discharge treatment for 1, 3, 5, and 8 min, the initial damage causes residual bacterial inactivation of 9.3, 37.2, 81.8, and 86.7%, respectively. Meanwhile, the discharge time and storage time in the different treatment processes can be optimized to achieve better bactericidal efficiency and energy efficiency. The results provide insights into the future development of plasma medicine and water purification.
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References
Maheux S, Duday D, Belmonte T, Penny C, Cauchie HM, Clement F, Choquet P (2015) Formation of ammonium in saline solution treated by nanosecond pulsed cold atmospheric microplasma: a route to fast inactivation of E-coli bacteria. Rsc Adv 5(52):42135–42140
Cheng C, Shen J, Xiao DZ, Xie HB, Lan Y, Fang SD, Meng YD, Paul KC (2014) Atmospheric pressure plasma jet utilizing Ar and Ar/H2O mixtures and its applications to bacteria inactivation. Chin Phys B 23(7):075024
Zhang XH, Liu DP, Wang HZ, Liu LY, Wang SB, Yang SZ (2012) Highly effective inactivation of Pseudomonas sp. HB1 in water by atmospheric pressure microplasma jet array. Plasma Chem Plasma Process 32(5):949–957
Ma Y, Chen JR, Yang B, Pu SC, Yu QS (2014) A study of plasma inactivation effects on Desulfovibrio bastinii in liquid using dielectric barrier discharge. IEEE Trans Plasma Sci 42(6):1607–1614
Naitali M, Herry JM, Hnatiuc E, Kamgang G, Brisset JL (2012) Kinetics and bacterial inactivation induced by peroxynitrite in electric discharges in air. Plasma Chem Plasma Process 32(4):675–692
Iseki S, Ohta T, Aomatsu A, Ito M, Kano H, Higashijima Y, Hori M (2010) Rapid inactivation of Penicillium digitatum spores using high-density nonequilibrium atmospheric pressure plasma. Appl Phys Lett 96(15):153704
Mai-Prochnow A, Murphy AB, McLean KM, Kong MG, Ostrikov K (2014) Atmospheric pressure plasmas: infection control and bacterial responses. Int J Antimicrob Agents 43(6):508–517
Dolezalova E, Lukes P (2015) Membrane damage and active but nonculturable state in liquid cultures of Escherichia coli treated with an atmospheric pressure plasma jet. Bioelectrochemistry 103:7–14
Xu Z, Shen J, Zhang Z, Ma J, Ma R, Zhao Y, Sun Q, Qian S, Zhang H, Ding L, Cheng C, Chu PK, Xia W (2015) Inactivation effects of non-thermal atmospheric-pressure helium plasma jet on Staphylococcus aureus biofilms. Plasma Process Polym 12(8):827–835
Iseki S, Hashizume H, Jia FD, Takeda K, Ishikawa K, Ohta T, Ito M, Hori M (2011) Inactivation of Penicillium digitatum spores by a high-density ground-state atomic oxygen-radical source employing an atmospheric-pressure plasma. Appl Phys Express 4(11):116201
Xin Q, Zhang XW, Lei LC (2008) Inactivation of bacteria in oil field injection water by non-thermal plasma treatment. Plasma Chem Plasma Process 28(6):689–700
Machala Z, Tarabova B, Hensel K, Spetlikova E, Sikurova L, Lukes P (2013) Formation of ROS vand RNS in water electro-sprayed through transient spark discharge in air and their bactericidal effects. Plasma Process Polym 10(7):649–659
Cheng C, Liu P, Xu L, Zhang LY, Zhan RJ, Zhang WR (2006) Development of a new atmospheric pressure cold plasma jet generator and application in sterilization. Chin Phys 15(7):1544–1548
Burlica R, Grim RG, Shih KY, Balkwill D, Locke BR (2010) Bacteria inactivation using low power pulsed gliding arc discharges with water spray. Plasma Process Polym 7(8):640–649
Lin A, Chernets N, Han J, Alicea Y, Dobrynin D, Fridman G, Freeman TA, Fridman A, Miller V (2015) Non-equilibrium dielectric barrier discharge treatment of mesenchymal stem cells: charges and reactive oxygen species play the major role in cell death. Plasma Process Polym 12(10):1117–1127
Panngom K, Baik KY, Nam MK, Han JH, Rhim H, Choi EH (2013) Preferential killing of human lung cancer cell lines with mitochondrial dysfunction by nonthermal dielectric barrier discharge plasma. Cell Death Dis 4(5):e642
Dobrynin D, Fridman G, Friedman G, Fridman A (2009) Physical and biological mechanisms of direct plasma interaction with living tissue. New J Phys 11(11):115020
Locke BR, Sato M, Sunka P, Hoffmann MR, Chang JS (2006) Electrohydraulic discharge and nonthermal plasma for water treatment. Ind Eng Chem Res 45(3):882–905
Lukes P, Clupek M, Babicky V, Spetlikova E, Sisrova I, Marsalkova E, Marsalek B (2013) High power DC diaphragm discharge excited in a vapor bubble for the treatment of water. Plasma Chem Plasma Process 33(1):83–95
Hsieh K, Wang HJ, Locke BR (2016) Analysis of a gas-liquid film plasma reactor for organic compound oxidation. J Hazard Mater 317:188–197
Bartis EAJ, Knoll AJ, Luan P, Seog J, Oehrlein GS (2016) On the interaction of cold atmospheric pressure plasma with surfaces of bio-molecules and model polymers. Plasma Chem Plasma Process 36(1):121–149
Onsuratoom S, Rujiravanit R, Sreethawong T, Tokura S, Chavadej S (2010) Silver loading on DBD plasma-modified woven PET surface for antimicrobial property improvement. Plasma Chem Plasma Process 30(1):191–206
Ikawa S, Kitano K, Hamaguchi S (2010) Effects of pH on bacterial inactivation in aqueous solutions due to low-temperature atmospheric pressure plasma application. Plasma Process Polym 7(1):33–42
Wu HY, Sun P, Feng HQ, Zhou HX, Wang RX, Liang YD, Lu JF, Zhu WD, Zhang J, Fang J (2012) 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. Plasma Process Polym 9(4):417–424
Bai N, Sun P, Zhou H, Wu H, Wang R, Liu F, Zhu W, Lopez JL, Zhang J, Fang J (2011) Inactivation of Staphylococcus aureus in water by a cold, He/O2 atmospheric pressure plasma microjet. Plasma Process Polym 8(5):424–431
Wang XQ, Wang FP, Chen W, Huang J, Bazaka K, Ostrikov KK (2016) Non-equilibrium plasma prevention of Schistosoma japonicum transmission. Sci Rep 6:35353
Oehmigen K, Hahnel M, Brandenburg R, Wilke C, Weltmann KD, von Woedtke T (2010) The role of acidification for antimicrobial activity of atmospheric pressure plasma in liquids. Plasma Process Polym 7(3–4):250–257
Lukes P, Dolezalova E, Sisrova I, Clupek M (2014) 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. Plasma Sources Sci Technol 23(1):015019
Lukes P, Locke BR, Brisset JL (2012) Aqueous-phase chemistry of electrical discharge plasma in water and in gas–liquid environments. In: Parvulescu VI, Magureanu M, Lukes P (eds) Plasma chemistry and catalysis in gases and liquids. Wiley-VCH, Weinheim, pp 241–307
Cheng H, Liu X, Lu XP, Liu DW (2016) Numerical study on propagation mechanism and bio-medicine applications of plasma jet. High Volt 1(2):62–73
Shen J, Sun Q, Zhang ZL, Cheng C, Lan Y, Zhang H, Xu ZM, Zhao Y, Xia WD, Chu PK (2015) Characteristics of DC gas–liquid phase atmospheric-pressure plasma and bacteria inactivation mechanism. Plasma Process Polym 12(3):252–259
Zhang H, Xu ZM, Shen J, Li X, Ding LL, Ma J, Lan Y, Xia WD, Cheng C, Sun Q, Zhang ZL, Chu PK (2015) Effects and mechanism of atmospheric-pressure dielectric barrier discharge cold plasma on lactate dehydrogenase (LDH) enzyme. Sci Rep-Uk 5:10031
Radu I, Bartnikas R, Wertheimer MR (2003) Frequency and voltage dependence of glow and pseudo glow discharges in helium under atmospheric pressure. IEEE Trans Plasma Sci 31(6):1363–1378
Hao YP, Chen JY, Yang L, Wang XL (2009) Lissajous figures of glow and filamentary dielectric barrier discharges under high frequency voltage at atmospheric pressure in helium. In: IEEE 2009: proceedings of the 9th international conference on properties and applications of dielectric materials, vols 1–3, pp 626–629
Du CM, Sun YW, Zhuang XF (2008) The effects of gas composition on active species and byproducts formation in gas-water gliding arc discharge. Plasma Chem Plasma Process 28(4):523–533
Burlica R, Kirkpatrick MJ, Locke BR (2006) Formation of reactive species in gliding arc discharges with liquid water. J Electrostat 64(1):35–43
Bruggeman P, Iza F, Lauwers D, Gonzalvo YA (2010) Mass spectrometry study of positive and negative ions in a capacitively coupled atmospheric pressure RF excited glow discharge in He–water mixtures. J Phys D Appl Phys 43(1):012003
Bian W, Zhou M, Lei L (2007) Formations of active species and by-products in water by pulsed high-voltage discharge. Plasma Chem Plasma Process 27(3):337–348
Graves DB (2012) The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. J Phys D Appl Phys 45(26):263001
van Gils CAJ, Hofmann S, Boekema BKHL, Brandenburg R, Bruggeman PJ (2013) Mechanisms of bacterial inactivation in the liquid phase induced by a remote RF cold atmospheric pressure plasma jet. J Phys D Appl Phys 46(17):175203
Bruggeman P, Iza F, Guns P, Lauwers D, Kong MG, Gonzalvo YA, Leys C, Schram DC (2010) Electronic quenching of OH(A) by water in atmospheric pressure plasmas and its influence on the gas temperature determination by OH(A–X) emission. Plasma Sources Sci Technol 19(1):015016
Nikiforov AY, Sarani A, Leys C (2011) The influence of water vapor content on electrical and spectral properties of an atmospheric pressure plasma jet. Plasma Sources Sci Technol 20(1):015014
Locke BR, Shih KY (2011) Review of the methods to form hydrogen peroxide in electrical discharge plasma with liquid water. Plasma Sources Sci Technol 20(3):034006
Graham WG, Stalder KR (2011) Plasmas in liquids and some of their applications in nanoscience. J Phys D Appl Phys 44(17):174037
Xiong Z, Lu XP, Feng A, Pan Y, Ostrikov K (2010) Highly effective fungal inactivation in He + O2 atmospheric-pressure nonequilibrium plasmas. Phys Plasmas 17(12):12305
Brisset JL, Benstaali B, Moussa D, Fanmoe J, Njoyim-Tamungang E (2011) Acidity control of plasma-chemical oxidation: applications to dye removal, urban waste abatement and microbial inactivation. Plasma Sources Sci Technol 20(3):034021
Tang YZ, Lu XP, Laroussi M, Dobbs FC (2008) Sublethal and killing effects of atmospheric-pressure, nonthermal plasma on eukaryotic microalgae in aqueous media. Plasma Process Polym 5(6):552–558
Lukes P, Brisset JL, Locke BR (2012) Biological effects of electrical discharge plasma in water and in gas-liquid environments. In: Parvulescu VI, Magureanu M, Lukes P (eds) Plasma chemistry and catalysis in gases and liquids. Wiley-VCH, Weinheim, pp 309–352
Yu H, Perni S, Shi JJ, Wang DZ, Kong MG, Shama G (2006) Effects of cell surface loading and phase of growth in cold atmospheric gas plasma inactivation of Escherichia coli K12[J]. J Appl Microbiol 101(6):1323–1330
Lu X, Ye T, Cao YG, Sun ZY, Xiong Q, Tang ZY, Xiong ZL, Hu J, Jiang ZH, Pan Y (2008) The roles of the various plasma agents in the inactivation of bacteria. J Appl Phys 104(5):053309
Shen J, Cheng C, Fang SD, Xie HB, Lan Y, Ni GH, Meng YD, Luo JR, Wang XK (2012) Sterilization of Bacillus subtilis spores using an atmospheric plasma jet with argon and oxygen mixture gas. Appl Phys Express 5(3):036201
Lu X, Naidis GV, Laroussi M, Reuter S, Graves DB, Ostrikov K (2016) Reactive species in non-equilibrium atmospheric-pressure plasmas: generation, transport, and biological effects. Phys Rep 630:1–84
Sun P, Sun Y, Wu HY, Zhu WD, Lopez JL, Liu W, Zhang J, Li RY, Fang J (2011) Atmospheric pressure cold plasma as an antifungal therapy. Appl Phys Lett 98(2):021501
Liu DX, Rong MZ, Wang XH, Iza F, Kong MG, Bruggeman P (2010) Main species and physicochemical processes in cold atmospheric-pressure He + O2 plasmas. Plasma Process Polym 7(9–10):846–865
Alkawareek MY, Gorman SP, Graham WG, Gilmore BF (2014) Potential cellular targets and antibacterial efficacy of atmospheric pressure non-thermal plasma. Int J Antimicrob Ag 43(2):154–160
Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112
Miller RA, Britigan BE (1997) Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 10(1):1–18
Yasuda H, Miura T, Kurita H, Takashima K, Mizuno A (2010) Biological evaluation of DNA damage in bacteriophages inactivated by atmospheric pressure cold plasma. Plasma Process Polym 7(3–4):301–308
Naitali M, Kamgang-Youbi G, Herry JM, Bellon-Fontaine MN, Brisset JL (2010) Combined effects of long-living chemical species during microbial inactivation using atmospheric plasma- treated water. Appl Environ Microb 76(22):7662–7664
Traylor MJ, Pavlovich MJ, Karim S, Hait P, Sakiyama Y, Clark DS, Graves DB (2011) Long-term antibacterial efficacy of air plasma-activated water. J Phys D Appl Phys 44(47):472001
Li LM, Zhang H, Huang Q (2015) New insight into the residual inactivation of Microcystis aeruginosa by dielectric barrier discharge. Sci Rep-Uk 5:13683
Acknowledgements
This work was supported jointly by the Science Foundation of Institute of Plasma Physics, Chinese Academy of Sciences No. DSJJ-14-YY02, National Natural Science Foundation of China under Grant No. 11475174, Natural Science Research Project of Anhui Province University No. KJ2015A327, as well as Hong Kong Research Grants Council (RGC) General Research Funds (GRF) No. CityU 11301215.
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Zhang, Z., Xu, Z., Cheng, C. et al. Bactericidal Effects of Plasma Induced Reactive Species in Dielectric Barrier Gas–Liquid Discharge. Plasma Chem Plasma Process 37, 415–431 (2017). https://doi.org/10.1007/s11090-017-9784-z
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DOI: https://doi.org/10.1007/s11090-017-9784-z