Atmospheric cold plasma inactivation of Escherichia coli in liquid media inside a sealed package

Journal of Applied Microbiology

Volumn 114, Issue 3, 2013, Pages 778-787

  Ziuzina, D ^a   Patil, S ^a   Cullen, P J ^a   Keener, K M ^b   Bourke, P ^a  

^a DUBLIN INSTITUTE OF TECHNOLOGY   (Ireland)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Atmospheric cold plasma; Dielectric barrier discharge; Escherichia coli; Inactivation efficacy; Ozone; Scanning electron microscopy

Indexed keywords

DIELECTRIC BARRIER DISCHARGE; DIELECTRIC DEVICES; DIELECTRIC MATERIALS; FLOW CONTROL; OZONE; PLASMA APPLICATIONS; SCANNING ELECTRON MICROSCOPY;

ATMOSPHERIC COLD PLASMA; COLD PLASMAS; DIELECTRIC BARRIER DISCHARGES; E. COLI; INACTIVATION EFFICACY; PLASMA DISCHARGE; POST TREATMENT; STORAGE TIME; SUSPENSION MEDIUM; TREATMENT TIME;

ESCHERICHIA COLI;

ALUMINUM; OZONE; PHOSPHATE BUFFERED SALINE;

ALUMINUM; COLIFORM BACTERIUM; DIELECTRIC PROPERTY; ELECTRODE; OZONE; PLASMA; SCANNING ELECTRON MICROSCOPY;

ARTICLE; ATMOSPHERIC PRESSURE; BACTERIAL CELL; CELL SUSPENSION; COLONY FORMING UNIT; CONTROLLED STUDY; DIELECTRIC BARRIER DISCHARGE ATMOSPHERIC COLD PLASMA; DISINFECTION; ELECTRODE; ESCHERICHIA COLI; MICROTITER PLATE ASSAY; NONHUMAN; PH; SCANNING ELECTRON MICROSCOPY; SEALED CONTAINER; SPECTROSCOPY; STORAGE; TEMPERATURE SENSITIVITY; TIME;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84873991282     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12087     Document Type: Article

References (44)

1. Arjunan, K.P. and Clyne, A.M. (2011) Hydroxyl radical and hydrogen peroxide are primarily responsible for dielectric barrier discharge plasma induced angiogenesis. Plasma Process Polym 8, 1154-1164.
2. Bárdos, L. and Barankova, H. (2010) Cold atmospheric plasma: sources, processes, and applications. Thin Solid Films 518, 6705-6713.
3. Bocci, V., Zanardi, I. and Travagli, V. (2011) Oxygen/ozone as a medical gas mixture. A critical evaluation of the various methods clarifies positive and negative aspects. Med Gas Res 1, 6.
4. Burlica, R., Kirkpatrick, M.J. and Locke, B.R. (2006) Formation of reactive species in gliding arc discharges with liquid water. J Electrostat 64, 35-43.
5. Chiper, A.S., Chen, W., Mejlholm, O., Dalgaard, P. and Stamate, E. (2011) Atmospheric pressure plasma produced inside a closed package by dielectric barrier discharge in Ar/CO2 for bacterial inactivation of biological samples. Plasma Sources Sci Technol 20, 10.
6. Chiang, M.H., Wu, J.Y., Li, Y.H., Wu, S., Chen, S.H. and Chang, C.L. (2010) Inactivation of E. coli and B. subtilis by a parallel-plate dielectric barrier discharge jet. Surf Coat Technol 204, 3729-3737.
7. Conrads, H. and Schmidt, M. (2000) Plasma generation and plasma sources. Plasma Sources Sci Technol 9, 441-454.
8. Cooper, M., Fridman, G., Fridman, A. and Joshi, S.G. (2010) Biological responses of Bacillus stratosphericus to floating electrode-dielectric barrier discharge plasma treatment. J Appl Microbiol 109, 2039-2048.
9. Du, C.M., Wang, J., Zhang, L., Li, H.X., Liu, H. and Xiong, Y. (2012) The application of a non-thermal plasma generated by gas - liquid gliding arc discharge in sterilization. New J Phys 14, 013010. doi: 10.1088/1367-2630/14/1/013010.
10. Ehlbeck, J., Schnabel, U., Polak, M., Winter, J., Woedtke, T., Brandenburg, R., Hagen, T. and Weltmann, K.D. (2011) Low temperature atmospheric pressure plasma sources for microbial decontamination. J Phys D: Appl Phys 44, 013002. doi: 10.1088/0022-3727/44/1/013002
11. Eto, H., Ono, Y., Ogino, A. and Nagatsu, M. (2008) Low-temperature sterilisation of wrapped materials using flexible sheet-type dielectric barrier discharge. Appl Phys Lett 93, 221502. doi: 10.1063/1.3039808
12. Fernandez, A. and Thompson, A. (2012) The inactivation of Salmonella by cold atmospheric plasma treatment. Food Res Int 45, 678-684.
13. Fernandez, A., Shearer, N., Wilson, D.R. and Thompson, A. (2012) Effect of microbial loading on the efficiency of cold atmospheric gas plasma inactivation of Salmonella entericaserovar Typhimurium. Int J Food Microbiol 152, 175-180.
14. Frohling, A., Baier, M., Ehlbeck, J., Knorr, D. and Schluter, O. (2012) Atmospheric pressure plasma treatment of Listeria innocua and Escherichia coli at polysaccharide surfaces: inactivation kinetics and flow cytometric characterisation. Innov Food Sci Emerg Technol 13, 142-150.
15. Gallagher, M.J., Vaze, J.N., Gangoli, S., Vasilets, V.N., Gustol, A.F., Milovanova, T.N., Anandan, S., Murasko, D.M. etal. (2007) Rapid inactivation of airborne bacteria using atmospheric pressure dielectric barrier grating discharge. IEEE Trans Plasma Sci 35, 1501-1510.
16. Green, A. K., Guzel-Seydim, Z. B. and Seydim, A. C. (2012) Chemical and physical properties of ozone. In Ozone in Food Processing ed. O'Donnel, C., Tiwary, B. K., Cullen, P. J. and Rice, R. G. pp. 26-28. UK: Blackwell Publishing Ltd.
17. Ikawa, S., Kitano, K. and Hamaguchi, S. (2010) Effect of pH on bacterial inactivation in aqueous solutions due to low-temperature atmospheric pressure plasma application. Plasma Processes Polym 7, 33-42.
18. Joshi, S.G., Cooper, M., Yost, A., Paff, M., Ercan, U.K., Fridman, G., Fridman, G., Fridman, A. etal. (2011) Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrob Agents Chemother 55, 1053-1062.
19. Julak, J., Scholtz, V., Kotucova, S. and Janouskova, O. (2012) The persistent microbiocidal effect in water exposed to the corona discharge. Phy Med 28, 230-239.
20. Kim, B., Yun, H., Jung, S., Jung, Y., Jung, H., Choe, W. and Jo, C. (2011) Effect of atmospheric pressure plasma on activation of pathogens inoculated onto bacon using two different gas compositions. Food Microbiol 28, 9-13.
21. Klockow, P.A. and Keener, K.M. (2009) Safety and quality assessment of packaged spinach treated with a novel ozone-generation system. LWT - Food Sci Technol 42, 1047-1053.
22. Kogelschatz, U. (2000) Fundamentals and applications of dielectric barrier discharges. Available at: http://www.coronalab.net/wxzl/plasma-16.pdf. [Accessed 12 March 2012].
23. Korachi, M., Gurol, C. and Aslan, N. (2010) Atmospheric plasma discharge sterilization effects on whole cell fatty acids profile of Escherichia coli and Staphylococcus aureus. J Electrostat 68, 508-512.
24. Laroussi, M. (2009) Low-temperature plasmas for medicine? Plasma Science. IEEE Trans Plasma Sci 37, 714-725.
25. Laroussi, M. and 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 Spectrom 233, 81-86.
26. Lee, H.J., Jung, H., Choe, W., Ham, J.S., Lee, J.H. and Jo, C. (2011) Inactivation of Listeria monocytogenes on agar and processed meat surfaces by atmospheric pressure plasma jets. Food Microbiol 28, 1468-1471.
27. Leipold, F., Schultz-Jensen, N., Kusano, Y., Bindslev, H. and Jacobsen, T. (2011) Decontamination of objects in a sealed container by means of atmospheric pressure plasmas. Food Control 22, 1296-1301.
28. Liu, F., Sun, P., Bai, N., Tia, Y., Zhou, H., Wei, S., Zhou, Y., Zhang, J. etal. (2010) Inactivation of bacteria in an aqueous environment by a direct-current, cold-atmospheric pressure air plasma microjet. Plasma Process Polym 7, 231-236.
29. Machala, Z., Janda, M., Hensel, K., Jedlovsky, I., Lestinska, L., Foltin, V., Martisovits, V. and Morvova, M. (2007) Emission spectroscopy of atmospheric pressure plasmas for bio-medical and environmental applications. J Mol Spectrosc 243, 194-201.
30. Miao, H. and Yun, G. (2011) The sterilisation of Escherichia coli by dielectric-barrier discharge plasma at atmospheric pressure. Appl Surf Sci 257, 7056-7070.
31. Misra, N.N., Tiwari, B.K., Raghavarao, K.S.M.S. and Cullen, P.J. (2011) Nonthermal plasma inactivation of food-borne pathogens. Food Eng Rev 3, 159-170.
32. Montie, T.C., Kelly-Wintenberg, K. and Roth, J.R. (2000) An overview of research using the one atmosphere uniform glow discharge plasma (OAUGDP) for sterilisation of surfaces and materials. IEEE Trans Plasma Sci 28, 1.
33. Moreau, M., Orange, N. and Feuilloley, M.G.J. (2008) Non-thermal plasma technologies: new tools for bio-decontamination. Biotechnol Adv 26, 610-617.
34. Mukhopadhyay, S. and Ramaswamy, R. (2012) Application of emerging technologies to control Salmonella in foods: a review. Food Res Int 45, 666-677.
35. Oehmigen, K., Hähnel, M., Brandenburg, R., Wilke, Ch., Weltmann, K.D. and Woedtke, T. (2010) The role of acidification for antimicrobial activity of atmospheric pressure plasma in liquids. Plasma Processes Polym 7, 250-257.
36. Patil, S., Valdramidis, V.P., Karatzas, K.A.G., Cullen, P.J. and Bourke, P. (2011) Assessing the microbial oxidative stress mechanism of ozone treatment through the responses of Escherichia coli mutants. J Appl Microbiol 111, 136-144.
37. Rod, S.K., Hansen, F., Leipold, F. and Knochel, S. (2012) Cold atmospheric pressure plasma treatment of ready-to-eat meat: inactivation of Listeria innocua and changes in productquality. Food Microbiol 30, 1-6.
38. Schwabedissen, A., Lacinski, P., Chen, X. and Engemann, J. (2007) PlasmaLabel - a new method to disinfect goods inside a closed package using dielectric barrier discharges. Contrib Plasma Phys 47, 551-558.
39. Song, H.P., Kim, B., Choe, J.H., Jung, S., Moon, S.S., Choe, W. and Jo, C. (2009) Evaluation of atmospheric pressure plasma to improve the safety of sliced cheese and ham inoculated by 3-strain cocktail Listeria monocytogenes. Food Microbiol 26, 432-436.
40. Tang, Y.Z., Lu, X.P., Laroussi, M. and Dobbs, F.C. (2008) Subletal and killing effects of atmospheric-pressure, non-thermal plasma on eukaryotic microalgae in aqueous media. Plasma Process Polym 5, 552-558.
41. Tendero, C., Tixier, C., Tristant, P., Desmaison, J. and Leprince, P. (2006) Atmospheric pressure plasmas: a review. Spectrochim Acta 61, 2-30.
42. Thanomsub, B., Anupunpisit, V., Chanphetch, S., Watcharachaipong, T., Poonkhum, R. and Srisukont, C. (2002) Effects of ozone treatment on cell growth and ultrastructural changes in bacteria. J Gen Appl Microbiol 48, 193-199.
43. Yu, H., Perni, S., Shi, J.J., Wang, D.Z., Kong, M.G. and Shama, G. (2006) Effects of cell surface loading and phase of growth in cold atmospheric gas plasma inactivation of Escherichia coli K12. J Appl Microbiol 101, 1323-1330.
44. Yun, H., Kim, B., Jung, S., Kruk, Z.A., Kim, D.B., Choe, W. and Jo, C. (2010) Inactivation of Listeria monocytogenes inoculated on disposable plastic tray, aluminium foil, and paper cup by atmospheric pressure plasma. Food Control 21, 1182-1186.