Skip to main content
SpringerLink
Log in

Helium atmospheric pressure plasma jet parameters and their influence on bacteria deactivation in a medium

  • Regular Article – Plasma Physics
  • Published:
The European Physical Journal D Aims and scope Submit manuscript

Abstract

Atmospheric pressure plasmas are becoming relevant in local microbial deactivation and other combined effects of plasmas on living organisms. For this reason, our research was focussed on optimisation of atmospheric pressure plasma jet (APPJ) parameters to complete the deactivation of different bacteria strains in a medium. Different helium APPJ treatments with different discharge parameters were used, such as input voltages and gas flows. To better understand plasma properties behind complete bacteria deactivation at optimised discharge parameters, optical and electrical plasma jet diagnostics were performed, including electrical characterisation of the plasma source, optical emission spectroscopy of the plasma plume and intensified charged coupled device imaging of the discharge behaviour for every set of plasma parameters. Then, the resulting plasma liquid chemistry was assessed to establish the connections between reactive species generated in the gaseous and liquid phases. The most efficient deactivation was found for higher discharge powers and gas flow rates, and that was linked to higher densities of reactive oxygen and nitrogen species, especially hydrogen peroxide and medium solvated charges.

Graphical abstract

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Data availability statement

This manuscript has no associated data or the data will not be deposited. [Authors’ comment: Data available on request from the authors - The data that support the findings of this study are available from the corresponding author, A. J., upon reasonable request.]

References

  1. Z. Dai, J. Ronholm, Y. Tian, B. Sethi, X. Cao, Sterilization techniques for biodegradable scaffolds in tissue engineering applications. J. Tissue Eng. 7, 204173141664881 (2016). https://doi.org/10.1177/2041731416648810

    Article  Google Scholar 

  2. J. Ehlbeck et al., Low temperature atmospheric pressure plasma sources for microbial decontamination. J. Phys. D Appl. Phys. (2011). https://doi.org/10.1088/0022-3727/44/1/013002

    Article  Google Scholar 

  3. R. Ben Gadri et al., Sterilization and plasma processing of room temperature surfaces with a one atmosphere uniform glow discharge plasma (OAUGDP). Surf. Coat. Technol. 131(1–3), 528–541 (2000). https://doi.org/10.1016/s0257-8972(00)00803-3

    Article  Google Scholar 

  4. P.M. Schneider, New technologies and trends in sterilization and disinfection. Am. J. Infect. Control 41(5 SUPPL.), S81–S86 (2013). https://doi.org/10.1016/j.ajic.2012.12.007

    Article  Google Scholar 

  5. A. Sakudo, Y. Yagyu, T. Onodera, Disinfection and sterilization using plasma technology: fundamentals and future perspectives for biological applications. Int. J. Mol. Sci. (2019). https://doi.org/10.3390/ijms20205216

    Article  Google Scholar 

  6. M. Laroussi, Nonthermal decontamination of biological media by atmospheric-pressure plasmas: review, analysis, and prospects. IEEE Trans. Plasma Sci. 30(4I), 1409–1415 (2002). https://doi.org/10.1109/TPS.2002.804220

    Article  ADS  Google Scholar 

  7. X. Liao et al., Bacterial spore inactivation induced by cold plasma. Crit. Rev. Food Sci. Nutr. 59(16), 2562–2572 (2019). https://doi.org/10.1080/10408398.2018.1460797

    Article  Google Scholar 

  8. H. Halfmann, B. Denis, N. Bibinov, J. Wunderlich, P. Awakowicz, Identification of the most efficient VUV/UV radiation for plasma based inactivation of Bacillus atrophaeus spores. J. Phys. D Appl. Phys. 40(19), 5907–5911 (2007). https://doi.org/10.1088/0022-3727/40/19/019

    Article  ADS  Google Scholar 

  9. S. Hofmann, Atmospheric pressure plasma jets - characterisation and interaction with human cells and bacteria, no. december. (2013)

  10. M. Keidar, E. Robert, Preface to special topic: plasmas for medical applications. Phys. Plasmas 22(12), 121901 (2015). https://doi.org/10.1063/1.4933406

    Article  ADS  Google Scholar 

  11. M. Keidar, D. Yan, I.I. Beilis, B. Trink, J.H. Sherman, Plasmas for treating cancer: opportunities for adaptive and self-adaptive approaches. Trends Biotechnol. 36(6), 586–593 (2018). https://doi.org/10.1016/j.tibtech.2017.06.013

    Article  Google Scholar 

  12. S. Schneider et al., The role of VUV radiation in the inactivation of bacteria with an atmospheric pressure plasma jet. Plasma Process. Polym. 9(6), 561–568 (2012). https://doi.org/10.1002/ppap.201100102

    Article  Google Scholar 

  13. N. Gopal, C. Hill, P.R. Ross, T.P. Beresford, M.A. Fenelon, P.D. Cotter, The prevalence and control of bacillus and related spore-forming bacteria in the dairy industry. Front. Microbiol. (2015). https://doi.org/10.3389/fmicb.2015.01418

    Article  Google Scholar 

  14. S. André, T. Vallaeys, S. Planchon, Spore-forming bacteria responsible for food spoilage. Res. Microbiol. 168(4), 379–387 (2017). https://doi.org/10.1016/j.resmic.2016.10.003

    Article  Google Scholar 

  15. S. Caulier, C. Nannan, A. Gillis, F. Licciardi, C. Bragard, J. Mahillon, Overview of the antimicrobial compounds produced by members of the bacillus subtilis group. Front. Microbiol. (2019). https://doi.org/10.3389/fmicb.2019.00302

    Article  Google Scholar 

  16. J. Vila et al., Escherichia coli: an old friend with new tidings. FEMS Microbiol. Rev. 40(4), 437–463 (2016). https://doi.org/10.1093/femsre/fuw005

    Article  MathSciNet  Google Scholar 

  17. J. Jang, H.-G. Hur, M.J. Sadowsky, M.N. Byappanahalli, T. Yan, S. Ishii, Environmental Escherichia coli: ecology and public health implications-a review. J. Appl. Microbiol. 123(3), 570–581 (2017). https://doi.org/10.1111/jam.13468

    Article  Google Scholar 

  18. T.J. Foster, J.A. Geoghegan, Staphylococcus aureus, in Molecular Medical Microbiology. (Elsevier, Amsterdam, 2015), pp. 655–674

    Google Scholar 

  19. S.Y.C. Tong, J.S. Davis, E. Eichenberger, T.L. Holland, V.G. Fowler, Staphylococcus aureus Infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 28(3), 603–661 (2015). https://doi.org/10.1128/CMR.00134-14

    Article  Google Scholar 

  20. S. Basak, P. Singh, M. Rajurkar, Multidrug resistant and extensively drug resistant bacteria: a study. J. Pathog. 2016, 1–5 (2016). https://doi.org/10.1155/2016/4065603

    Article  Google Scholar 

  21. L. Poirel et al., Antimicrobial resistance in Escherichia coli. Microbiol. Spectr. (2018). https://doi.org/10.1128/microbiolspec.ARBA-0026-2017

    Article  Google Scholar 

  22. M. Miletić et al., Inhibition of methicillin resistant Staphylococcus aureus by a plasma needle. Open Phys. (2014). https://doi.org/10.2478/s11534-014-0437-z

    Article  Google Scholar 

  23. A.H. Asghar, O.B. Ahmed, A.R. Galaly, Inactivation of E. Coli using atmospheric pressure plasma jet with dry and wet argon discharges. Membranes (Basel) 11(1), 1–20 (2021). https://doi.org/10.3390/membranes11010046

    Article  Google Scholar 

  24. A. Moldgy, G. Nayak, H.A. Aboubakr, S.M. Goyal, P.J. Bruggeman, Inactivation of virus and bacteria using cold atmospheric pressure air plasmas and the role of reactive nitrogen species. J. Phys. D Appl. Phys. 53(43), 434004 (2020). https://doi.org/10.1088/1361-6463/aba066

    Article  Google Scholar 

  25. J.-W. Lackmann, J.E. Bandow, Inactivation of microbes and macromolecules by atmospheric-pressure plasma jets. Appl. Microbiol. Biotechnol. 98(14), 6205–6213 (2014). https://doi.org/10.1007/s00253-014-5781-9

    Article  Google Scholar 

  26. C.A.J. van Gils, S. Hofmann, B.K.H.L. Boekema, R. Brandenburg, P.J. Bruggeman, Mechanisms of bacterial inactivation in the liquid phase induced by a remote RF cold atmospheric pressure plasma jet. J. Phys. D Appl. Phys. 46(17), 175203 (2013). https://doi.org/10.1088/0022-3727/46/17/175203

    Article  ADS  Google Scholar 

  27. F. Saadati, H. Mahdikia, H.A. Abbaszadeh, M.A. Abdollahifar, M.S. Khoramgah, B. Shokri, Comparison of Direct and Indirect cold atmospheric-pressure plasma methods in the B16F10 melanoma cancer cells treatment. Sci. Rep. 8(1), 1–15 (2018). https://doi.org/10.1038/s41598-018-25990-9

    Article  Google Scholar 

  28. S. Ikawa, K. Kitano, S. Hamaguchi, Effects of pH on bacterial inactivation in aqueous solutions due to low-temperature atmospheric pressure plasma application. Plasma Process. Polym. 7(1), 33–42 (2010). https://doi.org/10.1002/ppap.200900090

    Article  Google Scholar 

  29. S.M. Hosseini, B. Hosseinzadeh Samani, S. Rostami, Z. Lorigooini, Design and characterisation of jet cold atmospheric pressure plasma and its effect on Escherichia coli colour, pH, and bioactive compounds of sour cherry juice. Int. J. Food Sci. Technol. 56(10), 4883–4892 (2021). https://doi.org/10.1111/ijfs.15220

    Article  Google Scholar 

  30. V.S.S.K. Kondeti et al., Long-lived and short-lived reactive species produced by a cold atmospheric pressure plasma jet for the inactivation of Pseudomonas aeruginosa and Staphylococcus aureus. Free Radic. Biol. Med. 124, 275–287 (2018). https://doi.org/10.1016/j.freeradbiomed.2018.05.083

    Article  Google Scholar 

  31. A.L.V. Cubas et al., Effect of chemical species generated by different geometries of air and argon non-thermal plasma reactors on bacteria inactivation in water. Sep. Purif. Technol. 222, 68–74 (2019). https://doi.org/10.1016/j.seppur.2019.03.057

    Article  Google Scholar 

  32. P. Lukes, M. Clupek, V. Babicky, B. Pongrac, M. Simek, Bulk-phase chemistry induced by nanosecond discharge plasma in water. In: 2017 IEEE 19th International Conference on Dielectric Liquids (ICDL), (2017), pp. 1–3, https://doi.org/10.1109/ICDL.2017.8124702

  33. Y.S. Seo, A.A.H. Mohamed, K.C. Woo, H.W. Lee, J.K. Lee, K.T. Kim, Comparative studies of atmospheric pressure plasma characteristics between He and Ar working gases for sterilization. IEEE Trans. Plasma Sci. 38(10 PART 2), 2954–2962 (2010). https://doi.org/10.1109/TPS.2010.2058870

    Article  ADS  Google Scholar 

  34. E. Ilik, T. Akan, Optical properties of the atmospheric pressure helium plasma jet generated by alternative current (a.c.) power supply. Phys. Plasmas (2016). https://doi.org/10.1063/1.4948718

    Article  Google Scholar 

  35. A.N. Korbut, V.A. Kelman, Y.V. Zhmenyak, M.S. Klenovskii, Emission properties of an atmospheric-pressure helium plasma jet generated by a barrier discharge. Opt. Spectrosc. (English Transl. Opt. i Spektrosk.) 116(6), 919–925 (2014). https://doi.org/10.1134/S0030400X14040146

    Article  ADS  Google Scholar 

  36. J.J. Camacho, J.M.L. Poyato, L. Díaz, M. Santos, Optical emission studies of nitrogen plasma generated by IR CO2 laser pulses. J. Phys. B At. Mol. Opt. Phys. 40(24), 4573–4590 (2007). https://doi.org/10.1088/0953-4075/40/24/003

    Article  ADS  Google Scholar 

  37. S.J. Strickler, The identification of molecular spectra (Pearse, R. W. B.; Gaydon, A. G.). J. Chem. Educ. 41(5), A398 (1964). https://doi.org/10.1021/ed041pA398

    Article  Google Scholar 

  38. T. Darny, J.M. Pouvesle, J. Fontane, L. Joly, S. Dozias, E. Robert, Plasma action on helium flow in cold atmospheric pressure plasma jet experiments. Plasma Sources Sci. Technol. (2017). https://doi.org/10.1088/1361-6595/aa8877

    Article  Google Scholar 

  39. M. Foletto, V. Puech, J. Fontane, L. Joly, L.C. Pitchford, Evidence of the influence of plasma jets on a helium flow into open air. IEEE Trans. Plasma Sci. 42(10), 2436–2437 (2014). https://doi.org/10.1109/TPS.2014.2331393

    Article  ADS  Google Scholar 

  40. R. Zaplotnik, M. Bišćan, Z. Kregar, U. Cvelbar, M. Mozetič, S. Milošević, Influence of a sample surface on single electrode atmospheric plasma jet parameters. Spectrochim. Acta Part B At. Spectrosc. 103–104, 124–130 (2015). https://doi.org/10.1016/j.sab.2014.12.004

    Article  ADS  Google Scholar 

  41. P.J. Bruggeman et al., Plasma-liquid interactions: a review and roadmap. Plasma Sources Sci. Technol. (2016). https://doi.org/10.1088/0963-0252/25/5/053002

    Article  Google Scholar 

  42. Q. Xiong et al., Temporal and spatial resolved optical emission behaviors of a cold atmospheric pressure plasma jet. J. Appl. Phys. (2009). https://doi.org/10.1063/1.3239512

    Article  Google Scholar 

  43. G. Nersisyan, T. Morrow, W.G. Graham, Measurements of helium metastable density in an atmospheric pressure glow discharge. Appl. Phys. Lett. 85(9), 1487–1489 (2004). https://doi.org/10.1063/1.1784514

    Article  ADS  Google Scholar 

  44. G.V. Naidis, Production of active species in cold helium-air plasma jets. Plasma Sources Sci. Technol. (2014). https://doi.org/10.1088/0963-0252/23/6/065014

    Article  Google Scholar 

  45. R. Ono, Optical diagnostics of reactive species in atmospheric-pressure nonthermal plasma. J. Phys. D Appl. Phys. (2016). https://doi.org/10.1088/0022-3727/49/8/083001

    Article  Google Scholar 

Download references

Acknowledgements

This work was carried out within projects NATO SPS, and Slovenian Research Agency grant J4-1770. This article is also based upon work from COST Action PLAGRI—CA19110, supported by COST (European Cooperation in Science and Technology), www.cost.eu. K. S. acknowledges also partial funding from bilateral project Serbia-Slovenia from MESTD of Republic of Serbia. We thank Dr. Nevena Puac for useful advices related to electrical characterization.

Author information

Authors and Affiliations

  1. Jozef Stefan Institute, Jamova 39, 1000, Ljubljana, Slovenia

    Andrea Jurov, Martina Modic, Nataša Hojnik & Uroš Cvelbar

  2. Jozef Stefan International Postgraduate School, Jamova 39, 1000, Ljubljana, Slovenia

    Andrea Jurov & Uroš Cvelbar

  3. Institute of Physics, University of Belgrade, Pregrevica 118, Belgrade, 11080, Serbia

    Nikola Škoro & Kosta Spasić

  4. Center for Medical Microbiology, Institute of Public Health Montenegro, Dzona Dzeksona bb, 81000, Podgorica, Montenegro

    Danijela Vujošević & Milena Đurović

  5. Serbian Academy of Sciences and Arts, Knez Mihajlova 35, Belgrade, 11001, Serbia

    Zoran Lj. Petrović

  6. School of Engineering, Ulster University, York St., Belfast, BT15 1ED, UK

    Zoran Lj. Petrović

Authors
  1. Andrea Jurov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nikola Škoro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kosta Spasić
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martina Modic
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nataša Hojnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Danijela Vujošević
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Milena Đurović
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zoran Lj. Petrović
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Uroš Cvelbar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

UC and ZLP conceived and planned the experiments. NH, MM, DV and MĐ performed plasma treatment of bacteria and liquid chemistry analyses along with the interpretation of those results. NŠ, KS and AJ performed plasma diagnostics and electrical characterization along with interpretation of those results. AJ wrote the original draft, and all co-authors helped with manuscript revision.

Corresponding author

Correspondence to Andrea Jurov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jurov, A., Škoro, N., Spasić, K. et al. Helium atmospheric pressure plasma jet parameters and their influence on bacteria deactivation in a medium. Eur. Phys. J. D 76, 29 (2022). https://doi.org/10.1140/epjd/s10053-022-00357-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1140/epjd/s10053-022-00357-y

Search

Navigation