The European Physical Journal Special Topics

, Volume 226, Issue 13, pp 2887–2899

Reactive radical-driven bacterial inactivation by hydrogen-peroxide-enhanced plasma-activated-water

  • Songjie Wu
  • Qian Zhang
  • Ruonan Ma
  • Shuang Yu
  • Kaile Wang
  • Jue Zhang
  • Jing Fang
Regular Article
Part of the following topical collections:
  1. Technological Applications of Microplasmas


The combined effects of plasma activated water (PAW) and hydrogen peroxide (H2O2), PAW/HP, in sterilization were investigated in this study. To assess the synergistic effects of PAW/HP, S. aureus was selected as the test microorganism to determine the inactivation efficacy. Also, the DNA/RNA and proteins released by the bacterial suspensions under different conditions were examined to confirm membrane integrity. Additionally, the intracellular pH (pHi) of S. aureus was measured in our study. Electron spin resonance spectroscopy (ESR) was employed to identify the presence of radicals. Finally, the oxidation reduction potential (ORP), conductivity and pH were measured. Our results revealed that the inactivation efficacy of PAW/HP is much greater than that of PAW, while increased H2O2 concentration result in higher inactivation potential. More importantly, as compared with PAW, the much stronger intensity ESR signals and higher ORP in PAW/HP suggests that the inactivation mechanism of the synergistic effects of PAW/HP: more reactive oxygen species (ROS) and reactive nitrogen species (RNS), especially OH and NO radicals, are generated in PAW combined with H2O2 resulting in more deaths of the bacteria.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    S. Bekeschus, J. Kolata, C. Winterbourn, A. Kramer, R. Turner, K.D. Weltmann, B. Bröker, K. Masur, Free Rad. Res. 48, 5 (2014)CrossRefGoogle Scholar
  2. 2.
    T. Sato, M. Yokoyama, K. Johkura, J. Phys. D: Appl. Phys. 44, 372001 (2011)CrossRefGoogle Scholar
  3. 3.
    J. Winter, H. Tresp, M.U. Hammer, S. Iseni, S. Kupsch, A. Schmidt-Bleker, K. Wende, M. Dünnbier, K. Masur, K-D. Weltmann, S. Reuter, J. Phys. D: Appl. Phys. 47, 285401 (2014)CrossRefGoogle Scholar
  4. 4.
    S.K. Kang, M.Y. Choi, I.G. Koo, P.Y. Kim, Y. Kim, G.J. Kim, A.-A.H. Mohamed, G.J. Collins, J.K. Lee, Appl. Phys. Lett. 98, 143702 (2011)ADSCrossRefGoogle Scholar
  5. 5.
    H.W. Lee, G.J. Kim, J.M. Kim, J.K. Park, J.K. Lee, G.C. Kim, J. Endod 35, 587 (2009)CrossRefGoogle Scholar
  6. 6.
    M. Yamamoto, M. Nishioka, M. Sadakata, J. Electrostatics 56, 73 (2002)Google Scholar
  7. 7.
    I. Koban, M.H. Geisel, B. Holtfreter, L. Jablonowski, N.O. Hübner, R.M. KaiMasur, K.-D. Weltmann, A. Kramer, T. Kocher, ISRN Dentistry 2013, 573262 (2013)CrossRefGoogle Scholar
  8. 8.
    G. Kamgang-Youbi, J.-M. Herry, J.-L. Brisset, M.-N. Bellon-Fontaine, A. Doubla, M. Naïtali, Appl. Microbiol. Biotechnol. 81, 449 (2008)CrossRefGoogle Scholar
  9. 9.
    M. Naïtali, G. Kamgang-Youbi, J.-M. Herry, M.-N. Bellon-Fontaine, J.-L. Brisset, Appl. Environ. Microbiol. 76, 7662 (2010)CrossRefGoogle Scholar
  10. 10.
    G. Kamgang-Youbi, J.-M. Herry, T. Meylheuc, J.-L. Brisset, M.-N. Bellon-Fontaine, A. Doubla, M. Naïtali, Lett. Appl. Microbiol. 48, 13 (2009)CrossRefGoogle Scholar
  11. 11.
    M.J. Traylor, M.J. Pavlovich, S. Karim, P. Hait, Y. Sakiyama, D.S. Clark, D.B. Graves, J. Phys. D: Appl. Phys. 44, 472001 (2011)ADSCrossRefGoogle Scholar
  12. 12.
    K. Oehmigen, M. Hahnel, R. Brandenburg, Ch. Wilke, K.-D. Weltmann, Th. von Woedtke, Plasma Process. Polym. 7, 250 (2010)CrossRefGoogle Scholar
  13. 13.
    Q. Zhang, Y. Liang, H. Feng, R. Ma, Y. T. Jue Zhang, J. Fang, Appl. Phys. lett. 102, 203701 (2013)ADSCrossRefGoogle Scholar
  14. 14.
    S. Yu, Q. Chen, J. Liu, K. Wang, S. Sun, Z. Jiang, J. Zhang, J. Fang, Appl. Phys. Lett. 106, 244101 (2015)ADSCrossRefGoogle Scholar
  15. 15.
    B. Eliasson, U. Kogelschatz, IEEE Trans. Plasma Sci. 19, 1063 (1991)ADSCrossRefGoogle Scholar
  16. 16.
    J. Salge, Surf. Coat. Technol. 80, 1–7 (1996)CrossRefGoogle Scholar
  17. 17.
    M. Chen, S-L Huang, X-Q. Zhang, B. Zhang, H. Zhu, V.W. Yang, X-P. Zou, J. Cellular Biochem. 113, 2474 (2012)CrossRefGoogle Scholar
  18. 18.
    B. Halliwell, Plant Physiol. 141, 312 (2006)CrossRefGoogle Scholar
  19. 19.
    B. Halliwell, J. Gutteridge, Free Radicals in Biology and Medicine, 3rd ed. (Oxford University Press, 1999)Google Scholar
  20. 20.
    L.L. McPherson, Water Eng. Manage. 140, 29 (1993)Google Scholar
  21. 21.
    C.Z. Chen, S.L. Cooper, Biomaterials 23, 3359 (2002)CrossRefGoogle Scholar
  22. 22.
    J.S. Reidmiller, J.D. Baldeck, G.C. Rutherford, R.E. Marquis, J. Food Prot. 66, 1233 (2003)CrossRefGoogle Scholar
  23. 23.
    P.B.L. Chang, T.M. Young, Water Res. 34, 2233 (2000)CrossRefGoogle Scholar
  24. 24.
    O. Johansson, J. Bood, M. Aldén, U. Lindblad, Appl. Phys. B. 97, 515 (2009)ADSCrossRefGoogle Scholar
  25. 25.
    K.H. Cheeseman, T.F. Slater, Br. Med. Bull. 49, 481 (1993)CrossRefGoogle Scholar
  26. 26.
    G.V. Buxton, C.L. Greenstock, W.P. Helman, A.B. Ross, J. Phys. Chem. Ref. Data 17, 513 (1988)ADSCrossRefGoogle Scholar
  27. 27.
    R.P. Haugland, Eugene (OR): Molecular Probes, 6th edn. (1996)Google Scholar
  28. 28.
    F. Ullmann, Encyclopedia of Industrial Chemistry, 5th edn. (Verlag Chemie: Weinheim, 1989)Google Scholar
  29. 29.
    R.E. Kirk, D.F. Othmer, Encyclopedia of chemical technology, 4th ed. (Wiley-Interscience, London, 1995)Google Scholar
  30. 30.
    D.R. Lide, Strengths of chemical bond. 9, 51 (1999)Google Scholar
  31. 31.
    P. Bruggeman, D.C. Schram, Plasma Sources Sci. Technol. 19, 045025 (2010)ADSCrossRefGoogle Scholar
  32. 32.
    NIST Chemical Kinetic Database,
  33. 33.
    H.W.k. Lee, H.W. Lee, S.K. Kang, H.Y. Kim, I.H. Won, S.M. Jeon, J.K. Lee, Plasma Sources Sci. Technol. 22, 055008 (2013)ADSCrossRefGoogle Scholar
  34. 34.
    G. Merényi, J. Lind, S. Naumov, C. von Sonntag, Environ. Sci. Technol. 44, 3505 (2010)ADSCrossRefGoogle Scholar
  35. 35.
    C. Espírito Santo, N. Taudte, D.H. Nies, G. Grass, Appl. Environ. Microbiol. 74, 977 (2008)CrossRefGoogle Scholar
  36. 36.
    A.U. Khan, M. Kasha, Proc. Natl. Acad. Sci. 91, 12365 (1994)ADSCrossRefGoogle Scholar
  37. 37.
    B. Halliwell, J.M.C. Gutteridge, Biochem. J. 1, 210 (1984)Google Scholar
  38. 38.
    D.B. Graves, J. Phys. D: Appl. Phys. 45, 263001 (2012)ADSCrossRefGoogle Scholar
  39. 39.
    X. Hao, A.M. Mattson, C.M. Edelblute, M.A. Malik, L.C. Heller, J.F. Kolb, Plasma Process. Polym. 11, 1044 (2014)CrossRefGoogle Scholar
  40. 40.
    C.A.J. van Gils, S. Hofmann, B.K.H.L. Boekema, R. Brandenburg, P.J. Bruggeman, J. Phys. D: Appl. Phys. 46, 175203 (2013)ADSCrossRefGoogle Scholar
  41. 41.
    Y. Katsumura, The chemistry of free radicals in N-centered radicals (Wiley, Chichester, 1998), pp. 393–412Google Scholar
  42. 42.
    Y. Maeda, N. Igura, M. Shimoda, I. Hayakawa, Int. J. Food Sci. Technol. 38, 889 (2003)CrossRefGoogle Scholar
  43. 43.
    C.H. Foyer, J. Harbinson, P.M. Mullineaux, in Causes of photooxidative stress and amelioration of defense systems in plants (CRC Press, Boca Raton, 1994), pp. 1–42Google Scholar
  44. 44.
    B. Halliwell, Biochem. J. 163, 441 (1977)CrossRefGoogle Scholar
  45. 45.
    R. Mittlerand, B.A. Zilinskas, Plant Physiology 97, 962 (1991)CrossRefGoogle Scholar
  46. 46.
    G. Park, Y.H. Ryu, Y.J. Hong, E.H. Choi, H.S. Uhm, Appl. Phys. Lett. 100, 063703 (2012)ADSCrossRefGoogle Scholar
  47. 47.
    S.J. Kim, T.H. Chung, S.H. Bae, S.H. Leem, Appl. Phys. Lett. 94, 141502 (2009)ADSCrossRefGoogle Scholar
  48. 48.
    B.H.J. Bielski, D.E. Cabelli, R.L. Arudi, J. Phys. Chem. Ref. Data 14, 1041 (1985)ADSCrossRefGoogle Scholar
  49. 49.
    Q. Zhang, J. Zhuang, T. von Woedtke, J.F. Kolb, J. Zhang, J. Fang, K-D. Weltmann, Appl. Phys. Lett. 105, 104103 (2014)ADSCrossRefGoogle Scholar

Copyright information

© EDP Sciences and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Songjie Wu
    • 1
  • Qian Zhang
    • 2
  • Ruonan Ma
    • 2
  • Shuang Yu
    • 2
  • Kaile Wang
    • 2
  • Jue Zhang
    • 1
    • 2
  • Jing Fang
    • 1
    • 2
  1. 1.College of Engineering, Peking UniversityBeijingP.R. China
  2. 2.Academy for Advanced Interdisciplinary Studies, Peking UniversityBeijingP.R. China

Personalised recommendations