1887

Abstract

Non-thermal (low-temperature) physical plasma is under intensive study as an alternative approach to control superficial wound and skin infections when the effectiveness of chemical agents is weak due to natural pathogen or biofilm resistance. The purpose of this study was to test the individual susceptibility of pathogenic bacteria to non-thermal argon plasma and to measure the effectiveness of plasma treatments against bacteria in biofilms and on wound surfaces. Overall, Gram-negative bacteria were more susceptible to plasma treatment than Gram-positive bacteria. For the Gram-negative bacteria , and , there were no survivors among the initial 10 c.f.u. after a 5 min plasma treatment. The susceptibility of Gram-positive bacteria was species- and strain-specific. was the most resistant with 17 % survival of the initial 10 c.f.u. after a 5 min plasma treatment. had a strain-dependent resistance with 0 and 10 % survival from 10 c.f.u. of the Sa 78 and ATCC 6538 strains, respectively. and had medium resistance. Non-ionized argon gas was not bactericidal. Biofilms partly protected bacteria, with the efficiency of protection dependent on biofilm thickness. Bacteria in deeper biofilm layers survived better after the plasma treatment. A rat model of a superficial slash wound infected with and the plasma-sensitive strain Sa 78 was used to assess the efficiency of argon plasma treatment. A 10 min treatment significantly reduced bacterial loads on the wound surface. A 5-day course of daily plasma treatments eliminated from the plasma-treated animals 2 days earlier than from the control ones. A statistically significant increase in the rate of wound closure was observed in plasma-treated animals after the third day of the course. Wound healing in plasma-treated animals slowed down after the course had been completed. Overall, the results show considerable potential for non-thermal argon plasma in eliminating pathogenic bacteria from biofilms and wound surfaces.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.020263-0
2011-01-01
2024-11-08
Loading full text...

Full text loading...

/deliver/fulltext/jmm/60/1/75.html?itemId=/content/journal/jmm/10.1099/jmm.0.020263-0&mimeType=html&fmt=ahah

References

  1. Avetisian L. P., Chernukha M. Y., Gabrielian N. Y., Kovtun N. A., Gorskaia E. M., Shaginian I. A. 2009; Genotypic features of Pseudomonas aeruginosa strains circulating in surgical hospital. Zh Mikrobiol Epidemiol Immunobiol 5:33–38 (in Russian)
    [Google Scholar]
  2. Bland J. M., Altman D. G. 1996; Transformations, means, and confidence intervals. BMJ 312:1079 [CrossRef]
    [Google Scholar]
  3. Bogle M. A. 2006; Plasma skin regeneration technology. Skin Therapy Lett 11:7–9
    [Google Scholar]
  4. Brook I., Frazier E. H. 1998; Aerobic and anaerobic microbiology of infection after trauma. Am J Emerg Med 16:585–591 [CrossRef]
    [Google Scholar]
  5. Bukharin O. V., Valyshev A. V., Elagina N. N., Ivanov I. B., Cherkasov S. V. 1997; The photometric determination of the antilysozyme activity of microorganisms. Zh Mikrobiol Epidemiol Immunobiol 4:117–120 (in Russian)
    [Google Scholar]
  6. Calugaru A., Cremer L., Herold A., Lupu A., Szegli G., Lungu C., Lungu A., Georgescu N. 2005; The effect of the plasma needle on tumoral cell lines apoptosis. Roum Arch Microbiol Immunol 64:57–64
    [Google Scholar]
  7. Chang J. C., Ossoff S. F., Lobe D. C., Dorfman M. H., Dumais C. M., Qualls R. G., Johnson J. D. 1985; UV inactivation of pathogenic and indicator microorganisms. Appl Environ Microbiol 49:1361–1365
    [Google Scholar]
  8. Chau T. T., Kao K. C., Blank G., Madrid F. 1996; Microwave plasmas for low-temperature dry sterilization. Biomaterials 17:1273–1277 [CrossRef]
    [Google Scholar]
  9. Davey M. E., O'Toole G. A. 2000; Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867 [CrossRef]
    [Google Scholar]
  10. Elsaie M. L., Kammer J. N. 2008; Evaluation of plasma skin regeneration technology for cutaneous remodeling. J Cosmet Dermatol 7:309–311 [CrossRef]
    [Google Scholar]
  11. Hong Y. F., Kang J. G., Lee H. Y., Uhm H. S., Moon E., Park Y. H. 2009; Sterilization effect of atmospheric plasma on Escherichia coli and Bacillus subtilis endospores. Lett Appl Microbiol 48:33–37 [CrossRef]
    [Google Scholar]
  12. Hury S., Vidal D. R., Desor F., Pelletier J., Lagarde T. 1998; A parametric study of the destruction efficiency of Bacillus spores in low pressure oxygen-based plasmas. Lett Appl Microbiol 26:417–421 [CrossRef]
    [Google Scholar]
  13. Isbary G., Morfill G., Schmidt H. U., Georgi M., Ramrath K., Heinlin J., Karrer S., Landthaler M., Shimizu T. other authors 2010; A first prospective randomized controlled trial to decrease bacterial load using cold atmospheric argon plasma on chronic wounds in patients. Br J Dermatol 163:78–82
    [Google Scholar]
  14. Joaquin J. C., Kwan C., Abramzon N., Vandervoort K., Brelles-Mariño G. 2009; Is gas-discharge plasma a new solution to the old problem of biofilm inactivation?. Microbiology 155:724–732 [CrossRef]
    [Google Scholar]
  15. Kamgang J. O., Briandet R., Herry J. M., Brisset J. L., Naitali M. 2007; Destruction of planktonic, adherent and biofilm cells of Staphylococcus epidermidis using a gliding discharge in humid air. J Appl Microbiol 103:621–628 [CrossRef]
    [Google Scholar]
  16. Kaminskaya A., Pushkareva V., Moisenovich M., Stepanova T., Volkova N., Romanova J., Litvin V., Gintsburg A., Ermolaeva S. 2007; Stimulation of biofilm formation by insertion of Tetrahymena pyriformis wells within Burkholderia cenocepacia biofilms. Mol Gen Microbiol Virol 22:186–194 (erratum Mol Gen Microbiol Virol 23, 51 [CrossRef]
    [Google Scholar]
  17. 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. Foodborne Pathog Dis 4:50–59 [CrossRef]
    [Google Scholar]
  18. Kong M. G., Kroesen G., Morfill G., Nosenko T., Shimizu T., van Dijk J., Zimmermann J. L. 2009; Plasma medicine: an introductory review. New J Phys 11:115012 [CrossRef]
    [Google Scholar]
  19. Lassen K. S., Nordby B., Grün R. 2005; The dependence of the sporicidal effects on the power and pressure of RF-generated plasma processes. J Biomed Mater Res B Appl Biomater 74:553–559
    [Google Scholar]
  20. Lee K., Paek K., Ju W., Lee Y. 2006; Sterilization of bacteria, yeast, and bacterial endospores by atmospheric-pressure cold plasma using helium and oxygen. J Microbiol 44:269–275
    [Google Scholar]
  21. Lerouge S., Guignot C., Tabrizian M., Ferrier D., Yagoubi N., Yahia L. 2000a; Plasma-based sterilization: effect on surface and bulk properties and hydrolytic stability of reprocessed polyurethane electrophysiology catheters. J Biomed Mater Res 52:774–782 [CrossRef]
    [Google Scholar]
  22. Lerouge S., Wertheimer M. R., Marchand R., Tabrizian M., Yahia L. 2000b; Effect of gas composition on spore mortality and etching during low-pressure plasma sterilization. J Biomed Mater Res 51:128–135 [CrossRef]
    [Google Scholar]
  23. Lynch A. S., Robertson G. T. 2008; Bacterial and fungal biofilm infections. Annu Rev Med 59:415–428 [CrossRef]
    [Google Scholar]
  24. Millard M. M., Scherrer R., Thomas R. S. 1976; Surface analysis and depth profile composition of bacterial cells by x-ray photoelectron spectroscopy and oxygen plasma etching. Biochem Biophys Res Commun 72:1209–1217 [CrossRef]
    [Google Scholar]
  25. 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 Pharm 226:1–21 [CrossRef]
    [Google Scholar]
  26. Moreau M., Feuilloley M. G. J., Veron W., Meylheuc T., Chevalier S., Brisset J., Orange N. 2007; Gliding arc discharge in the potato pathogen Erwinia carotovora subsp. atroseptica : mechanism of lethal action and effect on membrane-associated molecules. Appl Environ Microbiol 73:5904–5910 [CrossRef]
    [Google Scholar]
  27. Moreau M., Orange N., Feuilloley M. G. J. 2008; Nonthermal plasma technologies: new tools for bio-decontamination. Biotechnol Adv 26:610–617 [CrossRef]
    [Google Scholar]
  28. 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 Microbiol 37:31–34 [CrossRef]
    [Google Scholar]
  29. Rice L. B. 2009; The clinical consequences of antimicrobial resistance. Curr Opin Microbiol 12:476–481 [CrossRef]
    [Google Scholar]
  30. Romanova I. M., Stepanova T. V., Nesterenko L. N., Balunets D. V., Andreev A. L., Shevliagina N. V., Borovaia T. G., Gintsburg A. L. 2009; Persistence of Burkholderia cenocepacia bacteria in vivo in dependence of their ability to form biofilms. Zh Mikrobiol Epidemiol Immunobiol 4:29–33 (in Russian)
    [Google Scholar]
  31. Rupf S., Lehmann A., Hannig M., Schäfer B., Schubert A., Feldmann U., Schindler A. 2010; Killing of adherent oral microbes by a nonthermal atmospheric plasma jet. J Med Microbiol 59:206–212 [CrossRef]
    [Google Scholar]
  32. Shaginian I. A., Khmel' I. A., Romanova I. M., Veselova M. A., Chernukha M. I., Chernin L. S., Sidorenko S. V., Lipasova V. A., Kovtun V. P. other authors 2003; Clinical strains of Burkholderia cepacia : characteristic and detection of the components in the quorum sensing regulatory system. Mol Gen Mikrobiol Virusol 4:15–20 (in Russian)
    [Google Scholar]
  33. Shaginian I. A., Kapranov N. I., Chernukha M. I., Alekseeva G. V., Semykin S. I., Avetisian L. R., Kashirskaia N. I., Pivkina N. V., Danilina G. A. other authors 2010; Microbial population of lower respiratory tract in children from different age groups with cystic fibrosis. Zh Mikrobiol Epidemiol Immunobiol 1:15–20 (in Russian)
    [Google Scholar]
  34. 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 [CrossRef]
    [Google Scholar]
  35. Sharp D. G. 1939; The lethal action of short ultraviolet rays on several common pathogenic bacteria. J Bacteriol 37:447–460
    [Google Scholar]
  36. Shimizu T., Steffes B., Pompl R., Jamitzky F., Bunk W., Ramrath K., Georgi M., Stolz W., Schmidt H.-U. other authors 2008; Characterization of microwave plasma torch for decontamination. Plasma Process Polym 5:577–582 [CrossRef]
    [Google Scholar]
  37. Strateva T., Yordanov D. 2009; Pseudomonas aeruginosa – a phenomenon of bacterial resistance. J Med Microbiol 58:1133–1148 [CrossRef]
    [Google Scholar]
  38. Takenaka S., Iwaku M., Hoshino E. 2001; Artificial Pseudomonas aeruginosa biofilms and confocal laser scanning microscopic analysis. J Infect Chemother 7:87–93 [CrossRef]
    [Google Scholar]
  39. Venezia R. A., Orrico M., Houston E., Yin S., Naumova Y. Y. 2008; Lethal activity of nonthermal plasma sterilization against microorganisms. Infect Control Hosp Epidemiol 29:430–436 [CrossRef]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.020263-0
Loading
/content/journal/jmm/10.1099/jmm.0.020263-0
Loading

Data & Media loading...

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