Original Article

Non-thermal plasma radiation-induced changes in antibiotic susceptibility and protein profile of Staphylococcus aureus


Background and Objectives: Plasma radiation is a widely used technique for sterilization or decontamination in various industries, as well as in some healthcare settings such as dentistry. The primary aim of this study was to assess the potential of plasma radiation to create a new population of Staphylococcus aureus cells with distinct characteristics that could lead to novel healthcare challenges.
Materials and Methods: A homemade non-thermal plasma apparatus was applied and the effects of plasma treatment on S. aureus ATCC25923 was assessed. Plasma radiation was applied under controlled conditions to ensure that some bacterial cells remained viable. The treatment was repeated 10 times, with each round followed by a recovery phase to collect any surviving bacterial cells. To assess the potential changes in the bacterial population, we examined the antibiotic susceptibility pattern, micro-structural characteristics using scanning electron microscopy (SEM), and total protein profile using the matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) technique.
Results: The experimental results revealed slight variations in the antibiotic susceptibility patterns of certain cell wall agents (imipenem, cephalothin, and cefepime), as well as in the MALDI-TOF spectra. However, no changes were observed in the SEM images.
Conclusion: The insufficient application of non-thermal plasma in bacterial decontamination may lead to physiological changes that could enrich or select certain subpopulations of S. aureus.

1. Niemira BA. Cold plasma decontamination of foods. Annu Rev Food Sci Technol 2012; 3: 125-142.
2. Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV. Fresh produce: A growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot 2004; 67: 2342-2353.
3. Thirumdas R, Sarangapani C, Annapure US. Cold Plasma: A novel non-thermal technology forf ood processing. Food Biophys 2015; 10: 1-11.
4. Bourke P, Ziuzina D, Boehm D, Cullen PJ, Keener K. The potential of cold plasma for safe and sustainable food production. Trends Biotechnol 2018; 36: 615-626.
5. Mir SA, Shah MA, Mir MM. Understanding the role of plasma technology in food industry. Food Bioprocess Technol 2016; 9: 734-750.
6. Misra NN, Tiwari BK, Raghavarao KSMS, Cullen PJ. Nonthermal plasma inactivation of food-borne pathogens. Food Eng Rev 2011; 3: 159-170.
7. Gomez E, Rani DA, Cheeseman CR, Deegan D, Wise M, Boccaccini AR. Thermal plasma technology for the treatment of wastes: A critical review. J Hazard Mater 2009; 161: 614-626.
8. Lu X, Cao Y, Yang P, Xiong Q, Xiong Z, Xian Y, et al. An RC plasma device for sterilization of root canal of teeth. IEEE Trans Plasma Sci 2009; 37: 668-673.
9. Zhang X, Huang J, Liu X, Peng L, Guo L, Lv G, et al. Treatment of Streptococcus mutans bacteria by a plasma needle. J Appl Phys 2009; 105: 063302.
10. Pasquali F, Stratakos AC, Koidis A, Berardinelli A, Cevoli C, Ragni L, et al. Atmospheric cold plasma process for vegetable leaf decontamination: A feasibility study on radicchio (red chicory, Cichorium intybus L.). Food Control 2016; 60: 552-559.
11. Burts ML, Alexeff I, Meek ET, McCullers JA. Use of atmospheric non-thermal plasma as a disinfectant for objects contaminated with methicillin-resistant Staphylococcus aureus. Am J Infect Control 2009; 37: 729-733.
12. Ekem N, Akan T, Akgun Y, Kiremitci A, Pat S, Musa G. Sterilization of Staphylococcus aureus by atmospheric pressure pulsed plasma. Surf Coat Technol 2006; 201: 993-997.
13. Park SR, Lee HW, Hong JW, Lee HJ, Kim JY, Choi BB, et al. Enhancement of the killing effect of low-temperature plasma on Streptococcus mutans by combined treatment with gold nanoparticles. J Nanobiotechnology 2014; 12: 29.
14. Critzer FJ, Kelly-Wintenberg K, South SL, Golden DA. Atmospheric plasma inactivation of foodborne pathogens on fresh produce surfaces. J Food Prot 2007; 70: 2290-2296.
15. Terrier O, Essere B, Yver M, Barthélémy M, Bouscambert-Duchamp M, Kurtz P, et al. Cold oxygen plasma technology efficiency against different airborne respiratory viruses. J Clin Virol 2009; 45: 119-124.
16. Lee K, Paek K-H, Ju W-T, Lee Y. Sterilization of bacteria, yeast, and bacterial endospores by atmospheric-pressure cold plasma using Helium and Oxygen. J Microbiol 2006; 44: 269-275.
17. Barekzi N, Laroussi M. Dose-dependent killing of leukemia cells by low-temperature plasma. J Phys D Appl Phys 2012; 45: 422002.
18. Ma R, Wang G, Tian Y, Wang K, Zhang J, Fang J. Non-thermal plasma-activated water inactivation of food-borne pathogen on fresh produce. J Hazard Mater 2015; 300: 643-651.
19. Kovalóvá Z, Zahoran M, Zahoranová A, Machala Z. Streptococci biofilm decontamination on teeth by low-temperature air plasma of dc corona discharges. J Phys D Appl Phys 2014; 47: 224014.
20. Mohd Nasir N, Lee BK, Yap SS, Thong KL, Yap SL. Cold plasma inactivation of chronic wound bacteria. Arch Biochem Biophys 2016; 605: 76-85.
21. Han L, Patil S, Boehm D, Milosavljević V, Cullen PJ, Bourke P. Mechanisms of inactivation by high-voltage atmospheric cold plasma differ for Escherichia coli and Staphylococcus aureus. Appl Environ Microbiol 2015; 82: 450-458.
22. Hosseini SI, Mohsenimehr S, Hadian J, Ghorbanpour M, Shokri B. Physico-chemical induced modification of seed germination and early development in artichoke (Cynara scolymus L.) using low energy plasma technology. Phys Plasmas 2018; 25: 013525.
23. Sobhani M, Abbas-Mohammadi M, Ebrahimi SN, Aliahmadi A. Tracking leading anti-Candida compounds in plant samples; Plumbago europaea. Iran J Microbiol 2018; 10: 187-193.
24. Moghimi R, Aliahmadi A, McClements DJ, Rafati H. Investigations of the effectiveness of nanoemulsions from sage oil as antibacterial agents on some food borne pathogens. LWT-Food Sci Technol 2016; 71: 69-76.
25. Böhme K, Fernández-No IC, Barros-Velázquez J, Gallardo JM, Cañas B, Calo-Mata P. SpectraBank: An open access tool for rapid microbial identification by MALDI-TOF MS fingerprinting. Electrophoresis 2012; 33: 2138-2142.
26. Winter T, Winter J, Polak M, Kusch K, Mäder U, Sietmann R, et al. Characterization of the global impact of low temperature gas plasma on vegetative microorganisms. Proteomics 2011; 11: 3518-3530.
27. Matthes R, Assadian O, Kramer A. Repeated applications of cold atmospheric pressure plasma does not induce resistance in Staphylococcus aureus embedded in biofilms. GMS Hyg Infect Control 2014; 9: Doc17.
28. Liao X, Li J, Suo Y, Ahn J, Liu D, Chen S, et al. Effect of preliminary stresses on the resistance of Escherichia coli and Staphylococcus aureus toward non-thermal plasma (NTP) challenge. Food Res Int 2018; 105: 178-183.
IssueVol 15 No 4 (2023) QRcode
SectionOriginal Article(s)
DOI https://doi.org/10.18502/ijm.v15i4.13508
Plasma radiation; Staphylococcus aureus; Modification; Mass spectrometry

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How to Cite
Rabbani-Esfahani M, Ghaderi L, Shali P, Ghassempour A, Hosseini SI, Aliahmadi A. Non-thermal plasma radiation-induced changes in antibiotic susceptibility and protein profile of Staphylococcus aureus. Iran J Microbiol. 2023;15(4):541-549.