Inactivation of microbes and macromolecules by atmospheric-pressure plasma jets

Applied Microbiology and Biotechnology

Volumn 98, Issue 14, 2014, Pages 6205-6213

  Lackmann, Jan Wilm ^a   Bandow, Julia Elisabeth ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Bacterial inactivation; Biomacromolecules; Clinical application; Cold atmospheric pressure plasma; Dielectric barrier discharge; Plasma jet

Indexed keywords

BACTERIA; IONIZATION OF GASES; PLASMA APPLICATIONS; PLASMA JETS;

ATMOSPHERIC PRESSURE PLASMAS; BACTERIAL INACTIVATION; BIOMACROMOLECULES; CLINICAL APPLICATION; DIELECTRIC BARRIER DISCHARGES;

PLASMAS;

ARGON; CATALASE; HELIUM; HYDROGEN PEROXIDE; NITRATE; NITRITE; NITROGEN; OXYGEN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE; DISINFECTANT AGENT; MACROMOLECULE; PLASMA GAS;

ATMOSPHERIC PRESSURE; BACTERIUM; BIODEGRADATION; DIELECTRIC PROPERTY; JET; MICROBIAL ACTIVITY; PATHOGEN; PLASMA; PUBLIC HEALTH; WOUNDING;

AIR POLLUTANT; ANGIOGENESIS; APOPTOSIS; ATMOSPHERIC PRESSURE; ATMOSPHERIC-PRESSURE PLASMA JET; BACTERIAL CELL; BACTERIAL INACTIVATION; BACTERIAL LOAD; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERICIDAL ACTIVITY; CELL PROLIFERATION; COLD; COLD ATMOSPHERIC PRESSURE PLASMA; DOUBLE STRANDED DNA BREAK; ELECTRODE; ENZYME INACTIVATION; ESCHERICHIA COLI; EUKARYOTIC CELL; GAS FLOW; HAILEY HAILEY DISEASE; IONIZATION; LEG ULCER; MACROMOLECULE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROORGANISM; NONHUMAN; OXIDATIVE STRESS; PHOTON; PLASMA GAS; PSEUDOMONAS AERUGINOSA; SHORT SURVEY; WOUND CLOSURE; WOUND HEALING; ANTAGONISTS AND INHIBITORS; BACTERIA; DRUG EFFECTS; MICROBIAL VIABILITY; PHARMACOLOGY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

ATMOSPHERIC PRESSURE; BACTERIA; DISINFECTANTS; MACROMOLECULAR SUBSTANCES; MICROBIAL VIABILITY; PLASMA GASES;

EID: 84903591667     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5781-9     Document Type: Short Survey

References (79)

1. Alberts B (2002) Molecular biology of the cell, 4th edn. Garland Science, New York
2. Alkawareek MY, Algwari QT, Laverty G, Gorman SP, Graham WG, O'Connell D, Gilmore BF, Vadivelu J (2012) Eradication of Pseudomonas aeruginosa biofilms by atmospheric pressure non-thermal plasma. PLoS ONE 7:e44289
3. Arjunan KP, Friedman G, Fridman A, Clyne AM (2012) Non-thermal dielectric barrier discharge plasma induces angiogenesis through reactive oxygen species. J R Soc Interface 9:147-157
4. Arndt S, Unger P, Wacker E, Shimizu T, Heinlin J, Li YF, Thomas HM, Morfill GE, Zimmermann JL, Bosserhoff AK, Karrer S (2013) Cold atmospheric plasma (CAP) changes gene expression of key molecules of the wound healing machinery and improves wound healing in vitro and in vivo. PLoS ONE 8:e79325
5. Becker KH (2005) Non-equilibrium air plasmas at atmospheric pressure. Institute of Physics Publishing, Bristol
6. Bekeschus S, Masur K, Kolata J, Wende K, Schmidt A, Bundscherer L, Barton A, Kramer A, Bröker B, Weltmann K (2013) Human mononuclear cell survival and proliferation is modulated by cold atmospheric plasma jet. Plasma Process Polym 10:706-713
7. Brehmer F, Haenssle HA, Daeschlein G, Ahmed R, Pfeiffer S, Görlitz A, Simon D, Schön MP, Wandke D, Emmert S (2014) 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). J Eur Acad Dermatol Venereol (in press)
8. Brullé L, Vandamme M, Riès D, Martel E, Robert E, Lerondel S, Trichet V, Richard S, Pouvesle J, Le Pape A (2012) Effects of a non thermal plasma treatment alone or in combination with gemcitabine in a MIA PaCa2-luc orthotopic pancreatic carcinoma model. PLoS ONE 7:e52653
9. Daeschlein G, von Woedtke T, Kindel E, Brandenburg R, Weltmann K, Jünger M (2010) Antibacterial activity of an atmospheric pressure plasma jet against relevant wound pathogens in vitro on a simulated wound environment. Plasma Process Polym 7:224-230
10. Deng X, Shi J, Kong M (2006) Physical mechanisms of inactivation of Bacillus subtilis spores using cold atmospheric plasmas. IEEE Trans Plasma Sci 34:1310-1316 (Pubitemid 44283326)
11. Deng XT, Shi JJ, Chen HL, Kong MG (2007) Protein destruction by a helium atmospheric pressure glow discharge: capability and mechanisms. Appl Phys Lett 90:13903
12. Dobrynin D, Wu A, Kalghatgi S, Park S, Shainsky N, Wasko K, Dumani E, Ownbey R, Joshi S, Sensenig R, Brooks AD (2011) Live pig skin tissue and wound toxicity of cold plasma treatment. Plasma Med 1: 93-108
13. 2 cold-plasma. Plasma Process Polym 9:612-618
14. Emmert S, Brehmer F, Hänßle H, Helmke A, Mertens N, Ahmed R, Simon D, Wandke D, Maus-Friedrichs W, Däschlein G, Schön MP, Viöl W (2013) Atmospheric pressure plasma in dermatology: ulcus treatment and much more. Clin Plasma Med 1:24-29
15. Fang M, Jin L, Zhang C, Tan Y, Jiang P, Ge N, Li H, Xing X, Sturtevant J (2013) 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. PLoS ONE 8:e77046
16. Fridman AA (2012) Plasma chemistry, reprint edition. Cambridge University Press, Cambridge
17. Fridman G, Shereshevsky A, Jost MM, Brooks AD, Fridman A, Gutsol A, Vasilets V, Friedman G (2007) Floating electrode dielectric barrier discharge plasma in air promoting apoptotic behavior in melanoma skin cancer cell lines. Plasma Chem Plasma Process 27:163-176 (Pubitemid 46501665)
18. Gaunt L, Beggs C, Georghiou G (2006) Bactericidal action of the reactive species produced by gas-discharge nonthermal plasma at atmospheric pressure: a review. IEEE Trans Plasma Sci 34:1257-1269 (Pubitemid 44283319)
19. Greenberg JT, Monach P, Chou JH, Josephy PD, Demple B (1990) Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc Natl Acad Sci U S A 87:6181-6185
20. Guénadou D, Lorcet H, Peybernès J, Catoire L, Osmont A, Gökalp I (2012) Plasma thermal conversion of bio-oil for hydrogen production. Int J Energy Res 36:409-414
21. Heinlin J, Morfill G, Landthaler M, Stolz W, Isbary G, Zimmermann JL, Shimizu T, Karrer S (2010) Plasma medicine: possible applications in dermatology. J Dtsch Dermatol Ges 8:968-976
22. Helmke A, Hoffmeister D, Mertens N, Emmert S, Schuette J, Vioel W (2009) The acidification of lipid film surfaces by non-thermal DBD at atmospheric pressure in air. New J Phys 11:115-125
23. Isbary G, Morfill G, Zimmermann J, Shimizu T, Stolz W (2011) Cold atmospheric plasma: a successful treatment of lesions in Hailey-Hailey disease. Arch Dermatol 147:388-390
24. Isbary G, Heinlin J, Shimizu T, Zimmermann JL, Morfill G, Schmidt H, Monetti R, Steffes B, Bunk W, Li Y, Klaempfl T, Karrer S, Landthaler M, Stolz W (2012) Successful and safe use of 2 min cold atmospheric argon plasma in chronic wounds: results of a randomized controlled trial. Br J Dermatol 167:404-410
25. Janzen G (1992) Plasmatechnik. Grundlagen, Anwendungen, Diagnostik. Hüthig Buch Verlag, Heidelberg
26. Kalghatgi SU, Fridman A, Friedman G, Clyne AM (2009) Cell proliferation following non-thermal plasma is related to reactive oxygen species induced fibroblast growth factor-2 release. Conf Proc IEEE Eng Med Biol Soc 2009:6030-6033
27. Kalghatgi S, Kelly CM, Cerchar E, Torabi B, Alekseev O, Fridman A, Friedman G, Azizkhan-Clifford J (2011) Effects of non-thermal plasma on mammalian cells. PLoS ONE 6:e16270
28. Kalghatgi S, Fridman A, Azizkhan-Clifford J, Friedman G (2012) DNA damage in mammalian cells by non-thermal atmospheric pressure microsecond pulsed dielectric barrier discharge plasma is not mediated by ozone. Plasma Process Polym 9:726-732
29. Keller S, Bibinov N, Neugebauer A, Awakowicz P (2013) Electrical and spectroscopic characterization of a surgical argon plasma discharge. J Phys D Appl Phys 46:25402
30. Kieft I, Kurdi M, Stoffels E (2006) Reattachment and apoptosis after plasma-needle treatment of cultured cells. IEEE Trans Plasma Sci 34:1331-1336 (Pubitemid 44283329)
31. Klämpfl TG, Isbary G, Shimizu T, Li Y, Zimmermann JL, Stolz W, Schlegel J, Morfill GE, Schmidt H (2012) Cold atmospheric air plasma sterilization against spores and other microorganisms of clinical interest. Appl Environ Microbiol 78:5077-5082
32. Kong MG, Kroesen G, Morfill G, Nosenko T, Shimizu T, van Dijk J, Zimmermann JL (2009) Plasma medicine: an introductory review. New J Phys 11:115012
33. Lackmann J, Schneider S, Narberhaus F, Benedikt J, Bandow JE (2012) Characterization of damage to bacteria and bio-macromolecules caused by (V)UV radiation and particles generated by a microscale atmospheric pressure plasma jet. In: Machala Z, Hensel K, Akishev Y (eds) Plasma for bio-decontamination, medicine and food security. Springer Netherlands, Dordrecht, pp 17-29
34. Lackmann J, Schneider S, Edengeiser E, Jarzina F, Brinckmann S, Steinborn E, Havenith M, Benedikt J, Bandow JE (2013) Photons and particles emitted from cold atmospheric-pressure plasma inactivate bacteria and biomolecules independently and synergistically. J R Soc Interface 10:20130591
35. Langmuir I (1928) Oscillations in ionized gases. Proc Natl Acad Sci U S A 14:627-637
36. Laroussi M (2005) Low temperature plasma-based sterilization: overview and state-of-the-art. Plasma Process Polym 2:391-400
37. Laroussi M, Leipold F (2004) Evaluation of the roles of reactive species, heat, and UV radiation in the inactivation of bacterial cells by air plasmas at atmospheric pressure. Int J Mass Spec 233:81-86
38. Leduc M, Guay D, Coulombe S, Leask RL (2010) Effects of non-thermal plasmas on DNA and mammalian cells. Plasma Process Polym 7: 899-909
39. Lee K, Joo Park B, Hee Lee D, Lee I, Hyun SO, Chung K, Park J (2005) Sterilization of Escherichia coli and MRSA using microwave-induced argon plasma at atmospheric pressure. Surf Coat Technol 193:35-38 (Pubitemid 40251951)
40. Lerouge S, Wertheimer M, Yahia L (2001) Plasma sterilization: a review of parameters, mechanisms, and limitations. Plasmas Polym 6:175-188 (Pubitemid 35401760)
41. Li Z, Demple B (1994) SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA. J Biol Chem 269:18371-18377
42. Lieberman MA, Lichtenberg AJ (2005) Principles of plasma discharges and materials processing, 2nd edn. Wiley-Interscience, Hoboken
43. Liebmann J, Scherer J, Bibinov N, Rajasekaran P, Kovacs R, Gesche R, Awakowicz P, Kolb-Bachofen V (2011) Biological effects of nitric oxide generated by an atmospheric pressure gas-plasma on human skin cells. Nitric Oxide 24:8-16
44. Locke BR, Shih K (2011) Review of the methods to form hydrogen peroxide in electrical discharge plasma with liquid water. Plasma Sources Sci Technol 20:34006
45. Lyman T (1914) Victor Schumann. Astrophys J 39:1
46. Maisch T, Shimizu T, Mitra A, Heinlin J, Karrer S, Li Y, Morfill G, Zimmermann JL (2012) Contact-free cold atmospheric plasma treatment of Deinococcus radiodurans. J Ind Microbiol Biotechnol 39: 1367-1375
47. Marschewski M, Hirschberg J, Omairi T, Höfft O, Viöl W, Emmert S, Maus-Friedrichs W (2012) Electron spectroscopic analysis of the human lipid skin barrier: cold atmospheric plasma-induced changes in lipid composition. Exp Dermatol 21:921-925
48. Noriega E, Shama G, Laca A, Díaz M, Kong MG (2011) Cold atmospheric gas plasma disinfection of chicken meat and chicken skin contaminated with Listeria innocua . Food Microbiol 28:1293-1300
49. O'Connell D, Cox LJ, Hyland WB, McMahon SJ, Reuter S, Graham WG, Gans T, Currell FJ (2011) Cold atmospheric pressure plasma jet interactions with plasmid DNA. Appl Phys Lett 98:43701
50. Oehmigen K, Hähnel M, Brandenburg R, Wilke C, Weltmann K, von Woedtke T (2010) The role of acidification for antimicrobial activity of atmospheric pressure plasma in liquids. Plasma Process Polym 7:250-257
51. Oehmigen K, Winter J, Hähnel M, Wilke C, Brandenburg R, Weltmann K, von Woedtke T (2011) Estimation of possible mechanisms of Escherichia coli inactivation by plasma treated sodium chloride solution. Plasma Process Polym 8:904-913
52. Park DP, Davis K, Gilani S, Alonzo C, Dobrynin D, Friedman G, Fridman A, Rabinovich A, Fridman G (2013) Reactive nitrogen species produced in water by non-equilibrium plasma increase plant growth rate and nutritional yield. Curr Appl Phys 13:S19
53. Partecke LI, Evert K, Haugk J, Doering F, Normann L, Diedrich S, Weiss F, Evert M, Huebner NO, Guenther C, Heidecke CD, Kramer A, Bussiahn R, Weltmann K, Pati O, Bender C, von Bernstorff W (2012) Tissue tolerable plasma (TTP) induces apoptosis in pancreatic cancer cells in vitro and in vivo . BMC Cancer 12:473
54. Perni S, Shama G, Hobman JL, Lund PA, Kershaw CJ, Hidalgo-Arroyo GA, Penn CW, Deng XT, Walsh JL, Kong MG (2007) Probing bactericidal mechanisms induced by cold atmospheric plasmas with Escherichia coli mutants. Appl Phys Lett 90:73902
55. Perni S, Liu DW, Shama G, Kong MG (2008) Cold atmospheric plasma decontamination of the pericarps of fruit. J Food Prot 71:302-308 (Pubitemid 351252827)
56. Ptasiñska S, Bahnev B, Stypczyñska A, Bowden M, Mason NJ, Braithwaite, Nicholas SJ (2010) DNA strand scission induced by a non-thermal atmospheric pressure plasma jet. Phys Chem Chem Phys 12:7779-7781
57. Quoc An HT, Pham Huu T, Le Van T, Cormier J, Khacef A (2011) Application of atmospheric non thermal plasma-catalysis hybrid system for air pollution control: Toluene removal. Catal Today 176:474-477
58. Radman M (1974) Phenomenology of an inducible mutagenic DNA repair pathway in Escherichia coli: SOS repair hypothesis. In: Sherman S, Miller M, Lawrence C, Tabor WH (eds) Molecular and environmental aspects of mutagenesis. Charcles C Thomas publisher, Springfield, pp 128-142
59. Schneider LA, Lorber A, Grabbe S, Dissemond J (2007) Influence of pH on wound-healing: a new perspective for wound-therapy? Arch Dermatol Res 298:413-420 (Pubitemid 46144202)
60. 2 atmospheric pressure plasma jet. J Phys D Appl Phys 44:295201
61. Schneider S, Lackmann J, Ellerweg D, Denis B, Narberhaus F, Bandow JE, Benedikt J (2012) The role of VUV radiation in the inactivation of bacteria with an atmospheric pressure plasma jet. Plasma Process Polym 9:561-568
62. Sharma A, Collins G, Pruden A (2009) Differential gene expression in Escherichia coli following exposure to nonthermal atmospheric pressure plasma. J Appl Microbiol 107:1440-1449
63. Sousa JS, Girard P, Sage E, Ravanat J, Puech V (2012) DNA oxidation by reactive oxygen species produced by atmospheric pressure microplasmas. In: Machala Z, Hensel K, Akishev Y (eds) Plasma for bio-decontamination, medicine and food security. Springer Netherlands, Dordrecht, pp 107-119
64. Stoffels E, Roks AJM, Deelman LE (2008a) Delayed effects of cold atmospheric plasma on vascular cells. Plasma Process Polym 5:599-605
65. Stoffels E, Sakiyama Y, Graves DB (2008b) Cold atmospheric plasma: charged species and their interactions with cells and tissues. IEEE Trans Plasma Sci 36:1441-1457
66. Takai E, Kitano K, Kuwabara J, Shiraki K (2012) Protein inactivation by low-temperature atmospheric pressure plasma in aqueous solution. Plasma Process Polym 9:77-82
67. Tanaka S, Horinouchi T, Abe S, Matsuno Y, Sasaki T, Kikuchi T, Harada N (2013) Inactivation property of microorganisms in water irradiated by atmospheric-pressure plasma using dielectric barrier discharge. IEEJ Trans Electr Electron Eng 8:105-110
68. Tresp H, Hammer MU, Winter J, Weltmann K, Reuter S (2013) Quantitative detection of plasma-generated radicals in liquids by electron paramagnetic resonance spectroscopy. J Phys D Appl Phys 46:435401
69. Trompeter F, Neff W, Franken O, Heise M, Neiger M, Liu S, Pietsch G, Saveljew A (2002) Reduction of Bacillus subtilis and Aspergillus niger spores using nonthermal atmospheric gas discharges. IEEE Trans Plasma Sci 30:1416-1423
70. 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 46:175203
71. Vandamme M, Robert E, Lerondel S, Sarron V, Ries D, Dozias S, Sobilo J, Gosset D, Kieda C, Legrain B, Pouvesle J, Le Pape A (2012) ROS implication in a new antitumor strategy based on non-thermal plasma. Int J Cancer 130:2185-2194
72. Wang L, Huang Z, Li G, Zhao H, Xing X, Sun W, Li H, Gou Z, Bao C (2010) Novel mutation breeding method for Streptomyces avermitilis using an atmospheric pressure glow discharge plasma. J Appl Microbiol 108:851-858
73. Winter T, Winter J, Polak M, Kusch K, Mäder U, Sietmann R, Ehlbeck J, van Hijum S, Weltmann K, Hecker M, Kusch H (2011) Characterization of the global impact of low temperature gas plasma on vegetative microorganisms. Proteomics 11:3518-3530
74. Winter T, Bernhardt J, Winter J, Mäder U, Schlüter R, Weltmann K, Hecker M, Kusch H (2013) Common versus noble: Bacillus subtilis differentially responds to air and argon gas plasma. Proteomics 13: 2608-2621
75. Woedtke T, Oehmigen K, Brandenburg R, Hoder T, Wilke C, Hähnel M, Weltmann K (2012) Plasma-liquid interactions: chemistry and antimicrobial effects. In: Machala Z, Hensel K, Akishev Y (eds) Plasma for bio-decontamination, medicine and food security. Springer Netherlands, Dordrecht, pp 67-78
76. Wolf RA (2012) Atmospheric pressure plasma for surface modification. Wiley-Blackwell, Hoboken
77. Wu H, Sun P, Feng H, Zhou H, Wang R, Liang Y, Lu J, Zhu W, 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 9:417-424
78. 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 Polym7:301-308
79. Zimmermann JL, Dumler K, Shimizu T, Morfill GE, Wolf A, Boxhammer V, Schlegel J, Gansbacher B, Anton M (2011) Effects of cold atmospheric plasmas on adenoviruses in solution. J Phys D Appl Phys 44:505201