Skip to main content

Advertisement

Log in

Inactivation of Staphylococcus aureus and Escherichia coli Biofilms by Air-Based Atmospheric-Pressure DBD Plasma

  • Original Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Air-based atmospheric-pressure plasma is an effective non-thermal method in deactivating various kinds of microbial biofilms with several advantages, including high bactericidal efficiency and low treatment costs. Bacterial biofilm formation is a major determinant in establishment of bacterial infection and also resistance to antibacterial chemotherapy. This study aims to assess the anti-biofilm potential of air-based atmospheric-pressure DBD plasma against Staphylococcus aureus and Escherichia coli biofilms. The biofilms of Staphylococcus aureus and Escherichia coli were exposed to air-based atmospheric-pressure DBD plasma for up to 4 min (control, 30 s, 90 s, 3 min, and 4 min) and their biofilm formation level, viability, and membrane integrity were determined. Based on the results, plasma exposure caused disruption up to 70% and 85% for S. aureus and E. coli biofilms, respectively. The biofilm disruption potential of air-based atmospheric-pressure DBD plasma was confirmed using the scanning electron microscopy (SEM). Besides, based on confocal laser scanning microscopy (CLSM), plasma exposure caused a significant bacterial inactivation and E. coli was found as more susceptible strain than S. aureus. In conclusion, atmospheric-pressure DBD plasma could be considered an efficient non-thermal approach against bacterial pathogenicity by biofilm disruption and thus prevention of infection establishment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

The data that supports the findings of this study are available within the article.

References

  1. Reyes, V. C., Opot, S. O., & Mahendra, S. (2014). Planktonic and biofilm grown nitrogen cycling bacteria exhibit different susceptibilities to copper nanoparticles. Environmental Toxicology and Chemistry, 34, 887–897.

    Article  CAS  Google Scholar 

  2. Montazeri, A., Salehzadeh, A., & Zamani, H. (2020). Effect of silver nanoparticles conjugated to thiosemicarbazide on biofilm formation and expression of intercellular adhesion molecule genes, icaAD, in Staphylococcus aureus. Folia Microbiologica, 65, 153–160.

    Article  CAS  PubMed  Google Scholar 

  3. Lahiri, D., Nag, M., Banerjee, R., Mukherjee, D., Garai, S., Sarkar, T., Dey, A., Sheikh, H. I., Pathak, S. K., Edinur, H. A., Pati, S., & Ray, R. R. (2021). Amylases: Biofilm inducer or biofilm inhibitor? Frontiers in Cellular and Infection Microbiology, 11, 660048.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Williamson, K. S., Richards, L. A., Perez-Osorio, A. C., Pitts, B., Mclnnerney, K., Stewart, Ph. S., & Farnklin, M. J. (2012). Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. Bacteriology, 194, 2062–2073.

    Article  CAS  Google Scholar 

  5. Gilmore, B. F., Flynn, P. B., O’Brien, S., Hickok, N., Freeman, Th., & Bourke, P. (2018). Cold plasmas for biofilm control: Opportunities and challenges. Trends in biotechnology, 36, 627–638.

    Article  CAS  PubMed  Google Scholar 

  6. Nag, M., Lahiri, D., Sarkar, T., Ghosh, S., Dey, A., AtanEdinur, H., Pati, S., & Ray, R. R. (2021). Microbial fabrication of nanomaterial and its role in disintegration of exopolymeric matrices of biofilm. Frontiers in Chemistry, 9, 690590.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Vuotto, C., & Donelli, G. (2019). Novel treatment strategies for bioflm-based infections. American Association of Pharmaceutical Scientists, 79, 1635–1655.

    CAS  Google Scholar 

  8. Nishime, T. M. C., Borges, A. C., Koga-Ito, C. Y., Machida, M., Hein, L. R. O., & Kostov, K. G. (2017). Non-thermal atmospheric pressure plasma jet applied to inactivation of different microorganisms. Surface and Coaching Technology, 312, 19–24.

    Article  CAS  Google Scholar 

  9. Julák, J., Vaňková, E., Válková, M., Kašparová, P., Masák, J., & Scholtz, V. (2020). Combination of non-thermal plasma and subsequent antibiotic treatment for biofilm re-development prevention. Folia Microbiologica, 65, 863–869.

    Article  PubMed  CAS  Google Scholar 

  10. Lahiri, D., Nag, M., Sheikh, H. I., Sarkar, T., Edinur, H. A., Pati, S., & Ray, R. R. (2021). Microbiologically-synthesized nanoparticles and their role in silencing the biofilm signaling cascade. Frontiers in Microbiology, 12, 636588.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Birmpa, A., Sfika, V., & Vantarakis, A. (2013). Ultraviolet light and ultrasound as non-thermal treatments for the inactivation of microorganisms in fresh ready-to-eat foods. Food Microbiology, 167, 96–102.

    Article  Google Scholar 

  12. Pereir, R. N., & Vicente, A. A. (2009). Environmental impact of novel thermal and non-thermal technologies in food processing. Food Research International, 43, 1936–1943.

    Article  Google Scholar 

  13. Gomez-Gomeza, A., Brito-de la Fuenteb, E., Gallegosb, C., Garcia-Pereza, J. V., & Benedito, J. (2020). Non-thermal pasteurization of lipid emulsions by combined supercritical carbon dioxide and high-power ultrasound treatment. Ultrasonics Sonochemistry, 67, 105138.

    Article  CAS  Google Scholar 

  14. Koban, I., Matthes, R., Hübner, N. O., Welk, A., Meisel, P., Holtfreter, B., & Sietmann, R. (2010). Treatment of Candida albicans biofilms with low-temperature plasma induced by dielectric barrier discharge and atmospheric pressure plasma jet. New Journal of Physics, 12, 073039.

    Article  CAS  Google Scholar 

  15. Li, Y., Xu, Y., Liao, Q., Xie, M., Tao, H., & Wang, H. L. (2021). Synergistic effect of hypocrellin B and curcumin on photodynamic inactivation of Staphylococcus aureus. Microbial Biotechnology, 14, 692–707.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Page, G. L., Gunnarsson, L., Snape, J., & Tyler, C. R. (2017). Integrating human and environmental health in antibiotic risk assessment: A critical analysis of protection goals, species sensitivity and antimicrobial resistance. Environment International, 109, 155–169.

    Article  PubMed  CAS  Google Scholar 

  17. Julák, J., Scholtz, V., & Vaňková, E. (2018). Medically important biofilms and non-thermal plasma. Applied Microbiology and Biotechnology, 34, 178.

    Google Scholar 

  18. Puligundla, P., & Mok, C. (2017). Potential applications of nonthermal plasmas against biofilm-associated micro-organisms in vitro. J. Applied Microbiology, 122, 1134–1148.

    Article  CAS  Google Scholar 

  19. Modica, M., Kovačb, J., Nichollsc, J. R., Kosd, Š, Seršad, G., Cvelbara, U., & Walsh, J. L. (2019). Targeted plasma functionalization of titanium inhibits polymicrobial biofilm recolonization and stimulates cell function. Applied Surface Science, 487, 1176–1188.

    Article  CAS  Google Scholar 

  20. Lunov, O., Zablotskii, V., Churpita, O., Jäger, A., Polívka, L., Syková, E., & Dejneka, A. (2016). The interplay between biological and physical scenarios of bacterial death induced by non-thermal plasma. Biomaterials, 82, 71–83.

    Article  CAS  PubMed  Google Scholar 

  21. Xu, Z., Shen, J., Zhang, Z., Ma, J., Ma, R., Zhao, Y., & Sun, Q. (2015). Inactivation effects of non-thermal atmospheric-pressure helium plasma jet on Staphylococcus aureus biofilms. Plasma Process and Polymers, 12, 827–835.

    Article  CAS  Google Scholar 

  22. Ehlbeck, J., Schnabel, U., Polak, M., Winter, J., Woedtke, Th. V., Brandenburg, R., dem Hagen, T. V., & Weltmann, K. D. (2011). Low temperature atmospheric pressure plasma sources for microbial decontamination. Journal of Applied Physics, 44, 013002.

    Google Scholar 

  23. Coutinho, N. M., Silveira, M. R., Rocha, R. S., Moraes, J., Ferreira, M. V. S., Pimentel, T. C., & Freitas, M. Q. (2018). Cold plasma processing of milk and dairy products. Trends in Food Science and Technology, 74, 56–68.

    Article  CAS  Google Scholar 

  24. Brandenburg, R., Ehlbeck, J., Stieber, M., Woedtke, T. V., Zeymer, J., Schluter, O., & Weltmann, K. D. (2007). Antimicrobial treatment of heat sensitive materials by means of atmospheric pressure Rf-driven plasma jet. Contributions to Plasma Physics, 47, 72–79.

    Article  CAS  Google Scholar 

  25. Lehmann, A., Pietag, F., & Arnold, Th. (2017). Human health risk evaluation of a microwave driven atmospheric plasma jet as medical device. Clinical Plasma Medicine, 7–8, 16–23.

    Article  Google Scholar 

  26. Dasan, B. G., Onal-Ulusoy, B., Pawlat, J., Diatczyk, J., Sen, Y., & Mutlu, M. (2016). A new and simple approach for decontamination of food contact surfaces with gliding arc discharge atmospheric non-thermal plasma. Food and Bioprocess Technology, 10, 650–661.

    Article  CAS  Google Scholar 

  27. Gupta, TTh., Matson, J. S., & Ayan, H. (2017). Antimicrobial effectiveness of regular dielectric barrier discharge (DBD) and jet DBD on the viability of Pseudomonas aeruginosa. IEEE Transactions on Radiation and Plasma Medical Sciences, 2, 68–76.

    Article  Google Scholar 

  28. Xu, Z., Shen, J., Cheng, Ch., Hu, Sh., Lan, Y., & Chu, P. K. (2017). Journal of Physics D: Applied Physics, 50, 105201.

    Article  CAS  Google Scholar 

  29. Ermolaeva, S. A., Varfolomeev, A. F., Chernukha, MYu., Yurov, D. S., Vasiliev, M. M., Kaminskaya, A. A., & Moisenovich, M. M. (2011). Bactericidal effects of non-thermal argon plasma in vitro, in biofilms and in the animal model of infected wounds. Medical of Microbiology, 60, 75–83.

    Article  CAS  Google Scholar 

  30. 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. J. Applied Microbiology, 48, 33–37.

    Article  CAS  Google Scholar 

  31. Hee Lee, M., Joo Park, B., Chang Jin, S., Kim, D., Han, I., Kim, J., & Hyun, S. O. (2009). Removal and sterilization of biofilms and planktonic bacteria by microwave-induced argon plasma at atmospheric pressure. New Journal of Physics, 11, 115022.

    Article  CAS  Google Scholar 

  32. Becker, K., Koutsospyros, A., Yin, S. M., Christodoulatos, C., Abramzon, N., Joaquin, J. C., & Brelles-Marino, G. (2005). Environmental and biological applications of microplasmas. Plasma Physics and Controlled Fusion, 47, 513–523.

    Article  CAS  Google Scholar 

  33. Vleugels, M., Shama, G., Deng, X. T., Greenacre, E., Brocklehurst, T., & Kong, M. G. (2005). Atmospheric plasma inactivation of biofilm-forming bacteria for food safety control. Plasma Science, 33, 824–828.

    Article  CAS  Google Scholar 

  34. Ulbin-Figlewicz, N., Brychcy, E., & Jarmoluk, A. (2015). Effect of low-pressure cold plasma on surface microflora of meat and quality attributes. Food Science and Technology, 52, 1228–1232.

    Google Scholar 

  35. Maisch, T., Shimizu, T., Isbary, G., Heinlin, J., Karrer, S., Klämpfl, T. G., & Li, Y.-F. (2012). Contact-free inactivation of Candida albicans biofilms by cold atmospheric air plasma. Applied and Environmental Microbiology, 78, 4242–4247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Govaert, M., Smet, C., Vergauwen, L., Ećimović, B., Walsh, J. L., Baka, M., & Van Impe, J. (2019). Influence of plasma characteristics on the efficacy of Cold Atmospheric Plasma (CAP) for inactivation of Listeria monocytogenes and Salmonella Typhimurium biofilms. Innovative Food Science and Emerging Technologies, 52, 376–386.

    Article  CAS  Google Scholar 

  37. Govaert, M., Smet, C., Graeffe, A., Walsh, J. L., & Van Impe, J. F. M. (2020). Inactivation of L. monocytogenes and S. typhimurium biofilms by means of an air-based cold atmospheric plasma (CAP) system. Foods, 9, 157.

    Article  CAS  PubMed Central  Google Scholar 

  38. Nilkar, M., Ghodsi, F. E., Jafari, S., Thiry, D., & Snyders, R. (2021). Effects of nitrogen incorporation on N-doped DLC thin film electrodes fabricated by dielectric barrier discharge plasma: Structural evolution and electrochemical performances. Journal of Alloys and Compounds, 853, 157298.

    Article  CAS  Google Scholar 

  39. Taghizadeh, L., Brackman, G., Nikiforov, A., van der Mullen, J., Leys, Ch., & Coenye, T. (2014). Inactivation of biofilms using a low power atmospheric pressure argon plasma jet; the role of entrained nitrogen. Plasma Process and Polymers, 12, 75–81.

    Article  CAS  Google Scholar 

  40. Graves, D. B., Bakken, L. B., Jensen, M. B., & Ingels, R. (2018). Plasma activated organic fertilizer. Plasma Chemistry and Plasma Processing, 39, 1–19.

    Article  CAS  Google Scholar 

  41. Joshi, S. G., Cooper, M., Yost, A., Paff, M., Ercan, U. K., Fridman, G., & Friedman, G. (2011). Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrobial Agents and Chemotherapy, 55, 1053–1063.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Tschang, C. Y. T., & Thoma, M. (2019). Biofilm inactivation by synergistic treatment of atmospheric pressure plasma and chelating agents. Clinical Plasma Medicine, 15, 100091.

    Article  Google Scholar 

  43. Lahiri, D., Dash, S., Dutta, R., & Nag, M. (2019). Elucidating the effect of anti-biofilm activity of bioactive compounds extracted from plants. Biosciences, 44, 52.

    Article  Google Scholar 

  44. Mangoudehi, H. T., Zamani, H., Shahangian, S. S., & Mirzanejad, L. (2020). Effect of curcumin on the expression of ahyI/R quorum sensing genes and some associated phenotypes in pathogenic Aeromonas hydrophila fish isolates. World Journal of Microbiology and Biotechnology, 36, 1–9.

    CAS  Google Scholar 

  45. Pei, X., Lu, X., Liu, J., Liu, D., Yang, Y., Ostrikov, K., Chu, P. K., & Pan, Y. (2012). Inactivation of a 25.5 μm Enterococcus faecalis biofilm by a room-temperature, battery-operated, handheld air plasma jet. Journal of Physics D: Applied Physics, 45, 1–5.

    Article  CAS  Google Scholar 

  46. Lahiri, D., Nag, M., Sarkar, T., Dutta, B., & Ray, R. R. (2021). Antibiofilm activity of α-amylase from Bacillus subtilis and prediction of the optimized conditions biofilm removal by response surface methodology (RSM) and artificial neural network (ANN). Applied Biochemistry and Biotechnology, 193, 1853–1872.

    Article  CAS  PubMed  Google Scholar 

  47. Bourke, P., Ziuzina, D., Han, L., Cullen, P. J., & Gilmore, B. F. (2017). Microbiological interactions with cold plasma. Journal of Applied Microbiology, 123, 308–324.

    Article  CAS  PubMed  Google Scholar 

  48. Lahiri, D., Nag, M., Dutta, B., Mukherjee, I., Ghosh, S., Dey, A., Banejee, R., & Ray, R. R. (2021). Catechin as the most efficient bioactive compound from Azadirachta indica with antibiofilm and anti-quorum sensing activities against dental biofilm: In vitro and in silico study. Applied Biochemistry and Biotechnology, 193, 1617–1630.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

S. Khosravi: investigation, methodology, writing—original draft. S. Jafari: methodology, supervision, review, and editing. H. Zamani: methodology, supervision, review, and editing. M. Nilkar: methodology, conceptualization, review, and editing.

Corresponding author

Correspondence to S. Jafari.

Ethics declarations

Ethics Approval

This article does not contain any studies with human participants performed by any of the authors.

Informed Consent

All authors declare that the current paper has not been under review by other journals, besides approving its submission on Applied Biochemistry and Biotechnology.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khosravi, S., Jafari, S., Zamani, H. et al. Inactivation of Staphylococcus aureus and Escherichia coli Biofilms by Air-Based Atmospheric-Pressure DBD Plasma. Appl Biochem Biotechnol 193, 3641–3650 (2021). https://doi.org/10.1007/s12010-021-03636-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-021-03636-3

Keywords

Navigation