1887

Abstract

Conventional disinfection and sterilization methods are often ineffective with biofilms, which are ubiquitous, hard-to-destroy microbial communities embedded in a matrix mostly composed of exopolysaccharides. The use of gas-discharge plasmas represents an alternative method, since plasmas contain a mixture of charged particles, chemically reactive species and UV radiation, whose decontamination potential for free-living, planktonic micro-organisms is well established. In this study, biofilms were produced using , a Gram-negative bacterium present in soil and water and used in this study as a model organism. Biofilms were subjected to an atmospheric pressure plasma jet for different exposure times. Our results show that 99.6 % of culturable cells are inactivated after a 5 min treatment. The survivor curve shows double-slope kinetics with a rapid initial decline in c.f.u. ml followed by a much slower decline with values that are longer than those for the inactivation of planktonic organisms, suggesting a more complex inactivation mechanism for biofilms. DNA and ATP determinations together with atomic force microscopy and fluorescence microscopy show that non-culturable cells are still alive after short plasma exposure times. These results indicate the potential of plasma for biofilm inactivation and suggest that cells go through a sequential set of physiological and morphological changes before inactivation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.021501-0
2009-03-01
2020-08-10
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/3/724.html?itemId=/content/journal/micro/10.1099/mic.0.021501-0&mimeType=html&fmt=ahah

References

  1. Abramzon N., Joaquin J. C., Bray J., Brelles-Mariño G.. 2006; Biofilm destruction by RF high-pressure cold plasma jet. IEEE Trans Plasma Sci IEEE Nucl Plasma Sci Soc34:1304–1309
    [Google Scholar]
  2. Akishev Y. S., Grushin M. E., Karal'nik V. B., Monich A. E., Pan'kin M. V., Trushkin N. I., Kholodenko V. P., Chugunov V. A., Zhirkova N. A.. other authors 2005; Sterilization/decontaminations of physiological solution and dry surface by non-thermal plasma created in bubbles and jet. In Proceedings of the 2nd International Workshop on Cold Atmospheric Pressure Plasmas pp69–72 ISBN: 908086692X;
    [Google Scholar]
  3. Becker K., Abramzon N., Panikov S., Crowe R., Ricatto P. J., Christodoulatos C.. 2002; Destruction of bacteria using an atmospheric-pressure dielectric capillary electrode discharge plasma. In Proceedings of the 29th International Conference on Plasma Science, Banff, Canada p253 ISBN: 0–7803–7407-X;
    [Google Scholar]
  4. Beringer J. E.. 1974; R factors transfer in Rhizobium leguminosarum. J Gen Microbiol84:188–198
    [Google Scholar]
  5. Brelles-Mariño G., Joaquin J. C., Bray J., Abramzon N.. 2005; Gas discharge plasma as a novel tool for biofilm destruction. In Proceedings of the 2nd International Workshop on Cold Atmospheric Pressure Plasmas pp69–72 ISBN: 908086692X;
    [Google Scholar]
  6. Colwell R. R., Huq A.. 1994; Vibrios in the environment: viable but nonculturable Vibrio cholerae. In Vibrio cholerae and Cholera: Molecular Global Perspectives Edited by Kaye T.. Washington DC: American Society for Microbiology;
    [Google Scholar]
  7. Conrads H., Schmidt M.. 2000; Plasma generation and plasma source. Plasma Sources Sci Technol9:441–454
    [Google Scholar]
  8. Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M.. 1995; Microbial biofilms. Annu Rev Microbiol49:711–745
    [Google Scholar]
  9. Costerton J. W., Stewart P. S., Greenberg E. P.. 1999; Bacterial biofilms: a common cause of persistent infections. Science284:1318–1322
    [Google Scholar]
  10. Critzer F. J., Kelly-Wintenberg K., South S. L., Golden D. A.. 2007; Atmospheric plasma inactivation of foodborne pathogens on fresh produce surfaces. J Food Prot70:2290–2296
    [Google Scholar]
  11. Davies D. G., Parske M. R., Pearson J. P., Iglewski B. H., Costerton J. W., Greenberg E. P.. 1998; The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science280:295–298
    [Google Scholar]
  12. Day A. P., Oliver J. D.. 2004; Changes in membrane fatty acid composition during entry of Vibrio vulnificus in the viable but nonculturable state. J Microbiol42:69–73
    [Google Scholar]
  13. De Kievit T. R., Gillis R., Marx S., Brown C., Iglewski B. H.. 2001; Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol67:1865–1873
    [Google Scholar]
  14. Du M., Chen J., Zhang X., Li A., Li Y., Wang Y.. 2007; Retention of virulence in a viable but nonculturable Edwardsiella tarda isolate. Appl Environ Microbiol73:1349–1354
    [Google Scholar]
  15. Elder M. J., Stapleton F., Evans E., Dart J. K.. 1995; Biofilm-related infections in ophthalmology. Eye9:102–109
    [Google Scholar]
  16. Ell S. R.. 1996; Candida, the cancer of silastic. J Laryngol Otol110:240–242
    [Google Scholar]
  17. Farr S. B., Kogoma T.. 1991; Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol Rev55:561–585
    [Google Scholar]
  18. Gallagher M., Friedman G., Gutsol A., Fridman A.. 2005; Non-thermal plasma application in air sterilization. In 17th International Symposium on Plasma Chemistry, Toronto, Canada pp1056–1057
    [Google Scholar]
  19. Halfmann H., Bibinov N., Wunderlich J., Awakowicz P.. 2007; A double inductively coupled plasma for sterilization of medical devices. J Phys D Appl Phys40:4145–4154
    [Google Scholar]
  20. Heydorn A., Nielsen A. T., Hentzer M., Sternberg C., Givskov M., Ersboll B. K., Molin S.. 2000; Quantification of biofilms structures by the novel computer program COMSTAT. Microbiology146:2395–2407
    [Google Scholar]
  21. Hoyle B. D., Costerton J. W.. 1991; Bacterial resistance to antibiotics: the role of biofilms. Prog Drug Res37:91–105
    [Google Scholar]
  22. ISO 1994; International Standard, ISO 11134. Sterilization of health care products. Requirements for validation and routine control – industrial moist heat sterilization.
  23. ISO 2000; International Standard, ISO 14937. Sterilization of health care products. General requirements for characterization of a sterilizing agent and the development, validation and routine control of a sterilization process for medical devices.
  24. Kamgang J. O., Briandet R., Herry J. M., Brisset J. L., Naïtali M.. 2007; Destruction of planktonic, adherent and biofilm cells of Staphylococcus epidermidis using a gliding discharge in humid air. J Appl Microbiol103:621–628
    [Google Scholar]
  25. Kayes M. M., Critzer F. J., Kelly-Wintenberg K., Roth J. R., Montie T. C., Golden D. A.. 2007; Inactivation of foodborne pathogens using a one atmosphere uniform glow discharge plasma (OAUGDP®. Foodborne Pathog Dis4:50–59
    [Google Scholar]
  26. Kelly-Wintenberg K., Montie T. C., Brickman C., Roth J. R., Tsai P. P. Y.. 1998; Room temperature sterilization of surfaces and fabrics with one atmosphere uniform glow discharge plasma. J Ind Microbiol Biotechnol20:69–74
    [Google Scholar]
  27. Kelly-Wintenberg K., Hodge A., Montie T. C., Deleanu L., Sherman D. M., Roth J. R., Tsai P., Wadsworth L.. 1999; Use of a one atmosphere uniform glow discharge plasma to kill a broad spectrum of microorganisms. J Vac Sci Technol A17:1539–1544
    [Google Scholar]
  28. Kelly-Wintenberg K., Sherman D. M., Tsai P. P.-Y., Gadri R. B., Karakaya F., Chen Z., Roth J. R., Montie T. C.. 2000; Air filter sterilization using a one atmosphere uniform glow discharge plasma (the volfilter). IEEE Trans Plasma Sci IEEE Nucl Plasma Sci Soc28:64–71
    [Google Scholar]
  29. Kolter R., Losick R.. 1998; One for all and all for one. Science280:226–227
    [Google Scholar]
  30. Laroussi M.. 1996; Sterilization of contaminated matter with an atmospheric pressure plasma. IEEE Trans Plasma Sci IEEE Nucl Plasma Sci Soc24:1188–1191
    [Google Scholar]
  31. Laroussi M.. 2002; Nonthermal decontamination of biological media by atmospheric-pressure plasmas: review, analysis, and prospects. IEEE Trans Plasma Sci IEEE Nucl Plasma Sci Soc30:1409–1415
    [Google Scholar]
  32. Laroussi M.. 2005; Low temperature plasma-based sterilization/decontamination of biological matter. In Proceedings of the 2nd International Workshop on Cold Atmospheric Pressure Plasmas pp18–27
    [Google Scholar]
  33. 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 Spectrom233:81–86
    [Google Scholar]
  34. Laroussi M., Alexeff I., Kang W.. 2000; Biological decontamination by non-thermal plasmas. IEEE Trans Plasma Sci IEEE Nucl Plasma Sci Soc28:184–188
    [Google Scholar]
  35. Laroussi M., Richardson J. P., Dobbs F. C.. 2001a; Biochemical pathways in the interaction of non-equilibrium plasma with bacteria. In Proceedings of ElectroMed 2001, 2nd International Symposium on Nonthermal Medical/Biological Treatments using Electromagnetic Fields, Portsmouth, VA, 20–23 May, 2001 pp33–34
    [Google Scholar]
  36. Laroussi M., Richardson J. P., Dobbs F. C.. 2001b; Biochemical and morphological effects of non-equilibrium atmospheric pressure plasmas on bacteria. In Proceedings of the 15th International Symposium on Plasma Chemistry (ISPC15), Orleans, France, July 9–13, 2001 pp729–734
    [Google Scholar]
  37. Leriche V., Briandet R., Carpentier B.. 2003; Ecology of mixed biofilms subjected daily to a chlorinated alkaline solution: spatial distribution of bacterial species suggests a protective effect of one species to another. Environ Microbiol5:64–71
    [Google Scholar]
  38. Lerouge S., Wertheimer M. R., Yahia L'H.. 2001; Plasma sterilization: a review of parameters, mechanisms, and limitations. Plasmas Polym6:175–188
    [Google Scholar]
  39. Marsh E. J., Luo H., Wang H.. 2003; A three-tiered approach to differentiate Listeria monocytogenes biofilm-forming abilities. FEMS Microbiol Lett228:203–210
    [Google Scholar]
  40. Matsumoto S., Terada A., Aoi Y., Tsuneda S., Alpkvist E., Picioreanu C., van Loosdrecht M. C. M.. 2007; Experimental and simulation analysis of community structure of nitrifying bacteria in a membrane-aerated biofilm. Water Sci Technol55:283–290
    [Google Scholar]
  41. Massol-Deyá A. A., Whallon J., Hickey R. F., Tiedje J. M.. 1995; Channel structures in aerobic biofilms of fixed-film reactors treating contaminated groundwater. Appl Environ Microbiol61:769–777
    [Google Scholar]
  42. McClean K. H., Winson M. K., Fish L., Taylor A., Chhabra S. R., Camara M., Daykin M., Lamb J. H., Swift S.. other authors 1997; Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology143:3703–3711
    [Google Scholar]
  43. Moisan M., Barbeau J., Moreau S., Pelletier J., Tabrizian M., Yahia L. H.. 2001; Low-temperature sterilization using gas plasmas: a review of the experiments and an analysis of the inactivation mechanisms. Int J Pharm226:1–21
    [Google Scholar]
  44. Moisan M., Barbeau J., Crevier M.-C., Pelletier J., Philip N., Saoudi B.. 2002; Plasma sterilization: methods and mechanisms. Pure Appl Chem74:349–358
    [Google Scholar]
  45. Montie C., Kelly-Wintenberg K., Roth J. R.. 2000; An overview of research using the one atmosphere uniform glow discharge plasma (OAUGDP) for sterilization of surfaces and materials. IEEE Trans Plasma Sci IEEE Nucl Plasma Sci Soc28:41–50
    [Google Scholar]
  46. Murga R., Stewart P. S., Daly D.. 1995; Quantitative analysis of biofilm thickness variability. Biotechnol Bioeng45:503–510
    [Google Scholar]
  47. Oliver J. D.. 1993; Formation of viable but nonculturable cells. In Starvation in Bacteria pp239–272 Edited by Kjelleberg S.. New York: Plenum Press;
    [Google Scholar]
  48. Panikov N. S., Paduraru S., Crowe R., Ricatto P. J., Christodoulatos C., Becker K.. 2002; Destruction of Bacillus subtilis cells using an atmospheric-pressure capillary plasma electrode discharge plasma. IEEE Trans Plasma Sci IEEE Nucl Plasma Sci Soc30:1424–1428
    [Google Scholar]
  49. Park B. J., Lee D. H., Park J. C., Lee I. S., Lee K. Y., Chun M. S., Chung K. H.. 2003; Sterilization using a microwave-induced argon plasma system at atmospheric pressure. Phys Plasmas10:4539–4544
    [Google Scholar]
  50. Park B. J., Takatori K., Lee M. H., Han D.-W., Woo Y. I., Son H. J., Kim J. K., Chung K.-H., Hyun S. O., Park J.-C.. 2007; Escherichia coli sterilization and lipopolysaccharide inactivation using microwave-induced argon plasma at atmospheric pressure. Surf Coat Tech201:5738–5741
    [Google Scholar]
  51. Picioreanu C., van Loosdrecht M. C. M., Heijnen J. J.. 2000; Modelling and predicting biofilm structure. In Community Structure and Co-operation in Biofilms pp129–166 Edited by Allison D. G., Gilbert P., Lappin-Scott H. M., Wilson M.. Cambridge, UK: Cambridge University Press;
    [Google Scholar]
  52. Purevdorj D., Igura N., Ariyada O., Hayakawa I.. 2003; Effect of feed gas composition of gas discharge plasmas on Bacillus pumilus spore mortality. Lett Appl Microbiol37:31–34
    [Google Scholar]
  53. Roszak D. B., Colwell R. R.. 1987; Survival strategies of bacteria in the natural environment. Microbiol Rev51:365–379
    [Google Scholar]
  54. Russo D. M., Williams A., Edwards A., Posadas D. M., Finnie C., Dankert M., Downie J. A., Zorreguieta A.. 2006; Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. J Bacteriol188:4474–4486
    [Google Scholar]
  55. Saravanan P., Nancharaiah Y. V., Venugopalan V. P., Rao T. S., Jayachandran S.. 2006; Biofilm formation by Pseudoalteromonas ruthenica and its removal by chlorine. Biofouling22:371–378
    [Google Scholar]
  56. Singh A., Singh H.. 1982; Time-scale and nature of radiation-biological damage: approaches to radiation protection and post-irradiation therapy. Prog Biophys Mol Biol39:69–107
    [Google Scholar]
  57. Stewart P. S.. 2002; Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol292:107–113
    [Google Scholar]
  58. Stewart P. S., Costerton J. W.. 2001; Antibiotic resistance of bacteria in biofilms. Lancet358:135–138
    [Google Scholar]
  59. Stewart P. S., Peyton B. M., Drury W. J., Murga R.. 1993; Quantitative observations of heterogeneities in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol59:327–329
    [Google Scholar]
  60. Stoodley P., Boyle J. D., Dodds I., Lappin-Scott H. M.. 1997; Consensus model of biofilm structure. In Biofilms: Community Interactions and Control pp1–9 Edited by Wimpenny J. W. T., Gilbert P. S., Lappin-Scott H. M., Jones M. Cardiff, UK: Bioline;
    [Google Scholar]
  61. Stoodley P., Sauer K., Davies D. G., Costerton J. W.. 2002; Biofilms as complex differentiated communities. Annu Rev Microbiol56:187–209
    [Google Scholar]
  62. Tolker Nielsen T., Brinch U. C., Ragas P. C., Andersen J. B., Jacobsen C. S., Molin S.. 2000; Development and dynamics of Pseudomonas sp. biofilms. J Bacteriol182:6482–6489
    [Google Scholar]
  63. Vandervoort K., Abramzon N., Brelles-Mariño G.. 2008; Plasma interactions with bacterial biofilms as visualized through atomic force microscopy. IEEE Trans Plasma Sci IEEE Nucl Plasma Sci Soc36:1296–1297
    [Google Scholar]
  64. Zimmermann R., Iturriaga R., Becker-Birek J.. 1978; Simultaneous determination of the total number of aquatic bacteria and the number thereof involved in respiration. Appl Environ Microbiol36:926–935
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.021501-0
Loading
/content/journal/micro/10.1099/mic.0.021501-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error