Advertisement

Medically important biofilms and non-thermal plasma

  • Jaroslav Julák
  • Vladimír Scholtz
  • Eva Vaňková
Review
  • 93 Downloads

Abstract

In recent decades, the non-thermal plasma, i.e. partially or completely ionized gas produced by electric discharges at ambient temperature, has become of interest for its microbiocidal properties with potential of use in the food industry or medicine. Recently, this interest focuses not only on the planktonic forms of microorganisms but also on their biofilms. The works in this interdisciplinary field are summarized in this review. The wide range of biofilm-plasma interactions is divided into studies of general plasma action on bacteria, on biofilm and on its oral and dental application; a short overview of plasma instrumentation is also included. In addition, not only biofilm combating but also an important area of biofilm prevention is discussed.

Graphical abstract

Various DC discharges of the point-to-plane type. Author’s photograph, published in Khun et al. (Plasma Sources Sci Technol 27:065002, 2018).

Keywords

Biofilm inactivation Biofilm prevention Dental and oral Non-thermal plasma production Wound healing 

Notes

Acknowledgements

This research was supported by the Charles University research program Progress Q25.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abdulsamee N (2017) Expanded tentacles of cold plasma energy in dentistry—review. EC Dent Sci 11 6:223–239. https://www.ecronicon.com/ecde/pdf/ECDE-11-00390.pdf
  2. Abramzon N, Joaquin JC, Bray J, Brelles-Mariño G (2006) Biofilm destruction by RF high-pressure cold plasma jet. IEEE Trans Plasma Sci 34:1304–1309.  https://doi.org/10.1109/TPS.2006.877515 CrossRefGoogle Scholar
  3. Akishev Y, Grushin M, Karalnik V, Trushkin N, Kholodenko V, Chugunov V, Kobzev E, Zhirkova N, Irkhina I, Kireev G (2008) Atmospheric-pressure, nonthermal plasma sterilization of microorganisms in liquids and on surfaces. Pure Appl Chem 80:1953–1969.  https://doi.org/10.1351/pac200880091953 CrossRefGoogle Scholar
  4. Alkawareek MY, Algwari QT, Gorman SP, Graham WG, O’Connell D, Brendan F, Gilmore BF (2012) Application of atmospheric pressure nonthermal plasma for the in vitro eradication of bacterial biofilms. FEMS Immunol Med Microbiol 65:381–384.  https://doi.org/10.1111/j.1574-695X.2012.00942.x CrossRefPubMedGoogle Scholar
  5. Alkawareek M, Gorman S, Graham B, Gilmore B (2013) Microscopic examination of biofilm destruction by atmospheric pressure plasma. Eurobiofilms 2013–3rd European congress on microbial biofilms, Ghent, Belgium. 09 Sep.–12 Sep. 2013, p. 53. https://pure.qub.ac.uk/portal/en/publications/microscopic-examination-of-biofilm-destruction-by-atmospheric-pressure-plasma(7a571701-984b-40fb-a458-c4bce60b0cd7).html
  6. Boehm D, Curtin J, Cullen PJ, Bourke P (2017) Hydrogen peroxide and beyond - the potential of high-voltage plasma-activated liquids against cancerous cells. Anti-cancer Agents Med Chem 17:1–9.  https://doi.org/10.2174/1871520617666170801110517 CrossRefGoogle Scholar
  7. Boudam MK, Moisan M, Saoudi B, Popovici C, Massines F (2006) Bacterial spore inactivation by atmospheric-pressure plasmas in the presence or absence of UV photons as obtained with the same gas mixture. J Phys D 39::3494–3507.  https://doi.org/10.1088/0022-3727/39/16/S07 CrossRefGoogle Scholar
  8. Bourke P, Ziuzina D, Han L, Cullen PJ, Gilmore BF (2017) Microbiological interactions with cold plasma. J Appl Microbiol 123:308–324.  https://doi.org/10.1111/jam.13429 CrossRefPubMedGoogle Scholar
  9. Brelles-Mariño G (2012) Challenges in Biofilm Inactivation: The Use of Cold Plasma as a New Approach. J Bioproces Biotechniq 2:1000e107.  https://doi.org/10.4172/2155-9821.1000e107 CrossRefGoogle Scholar
  10. Brelles-Mariño G (2016) Gas-discharge plasma: biofilm inactivation. In: Encyclopedia of plasma technology, 1st edn. CRC Press, Taylor & Francis, Boca Raton.  https://doi.org/10.1081/E-EPLT-120050769 CrossRefGoogle Scholar
  11. Carmen JC, Roeder BL, Nelson JL, Ogilvie RLR, Robison RA, Schaalje GB, Pitt WG (2005) Treatment of biofilm infections on implants with low-frequency ultrasound and antibiotics. Am J Infect Control 33(5):78–82.  https://doi.org/10.1016/j.ajic.2004.08.002 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Carmona-Gutierrez D, Eisenberg T, Büttner S, Meisinger C, Kroemer G, Madeo F (2010) Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ 17:763–773.  https://doi.org/10.1038/cdd.2009.219 CrossRefPubMedGoogle Scholar
  13. Cha S, Park Y-S (2014) Plasma in dentistry. Clin Plasma Med 2:4–10.  https://doi.org/10.1016/j.cpme.2014.04.002 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chen C, Liu DX, Liu ZC, Yang AJ, Chen HL, Shama G, Kong MC (2014) A model of plasma-biofilm and plasma-tissue interactions at ambient pressure. Plasma Chem Plasma Process 34:403–441.  https://doi.org/10.1007/s11090-014-9545-1 CrossRefGoogle Scholar
  15. Cheng H. Xin L, Lu X. Liu D (2016) Active species delivered by dielectric barrier discharge filaments to bacteria biofilms on the surface of apple. Phys Plasmas 23:073517.  https://doi.org/10.1063/1.4955323 CrossRefGoogle Scholar
  16. Cheruthazhekatt S, Černák M, Slavíček P, Havel J (2010) Gas plasmas and plasma modified materials in medicine. J Appl Biomed 8:55–66.  https://doi.org/10.2478/v10136-009-0013-9 CrossRefGoogle Scholar
  17. Chizoba Ekezie F-G, Sun D-W, Cheng J-H (2017) A review on recent advances in cold plasma technology for the food industry: Current applications and future trends. Trends Food Sci Technol 69:46–58.  https://doi.org/10.1016/j.tifs.2017.08.007 CrossRefGoogle Scholar
  18. Cotter JJ, Maguire P, Soberon F, Daniels S, O’Gara JP, Casey E (2011) Disinfection of meticillin-resistant Staphylococcus aureus and Staphylococcus epidermidis biofilms using a remote non-thermal gas plasma. J Hosp Infect 78:204–207.  https://doi.org/10.1016/j.jhin.2011.03.019 CrossRefPubMedGoogle Scholar
  19. Czapka T, Maliszewska I, Olesiak-Bańska J (2018) Influence of atmospheric pressure non-thermal plasma on inactivation of biofilm cells. Plasma Chem Plasma Process.  https://doi.org/10.1007/s11090-018-9925-z, in pressCrossRefGoogle Scholar
  20. Daeschlein G, Scholz S, von Woedtke T, Niggemeier M, Kindel E, Brandenburg R, Weltmann K-D, Junger M (2011) In vitro killing of clinical fungal strains by low-temperature atmospheric-pressure plasma jet. IEEE Trans Plasma Sci 39:815–821.  https://doi.org/10.1109/TPS.2010.2063441 CrossRefGoogle Scholar
  21. de Sousa LAF, Marques DM, Monteiro RM, Francisco AA, Queiroz L, Andrade D, Watanabe E (2017) Prevention of biofilm formation on artificial pacemakers: is it feasible? Acta Paulista de Enferm 30:644–650.  https://doi.org/10.1590/1982-0194201700085 CrossRefGoogle Scholar
  22. Delben JA, Zago CE, Tyhovych N, Duarte S, Vergani CE (2016) Effect of atmospheric-pressure cold plasma on pathogenic oral biofilms and in vitro reconstituted oral epithelium. PLoS ONE 11:e0155427.  https://doi.org/10.1371/journal.pone.0155427 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Denes AR, Somers EB, Lee Wong AC, Denes FS (2000) Plasma-aided treatment of surfaces against bacterial attachment and biofilm deposition. United States Patent Number 6,096,564. Aug. 1,Google Scholar
  24. Dhanasekaran D, Thajuddin N (eds) (2016) Microbial biofilms—importance and applications. InTech. ISBN 978-953-51-2435-1Google Scholar
  25. Dobrynin D, Friedman G, Fridman A, Starikovskiy A (2011) Inactivation of bacteria using dc corona discharge: role of ions and humidity. New J Phys 13:103033.  https://doi.org/10.1088/1367-2630/13/10/103033 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Donelli G (ed) (2014) Microbial biofilms. Methods and protocols. Springer, New York. ISBN 978-1-4939-0467-9Google Scholar
  27. Ehlbeck J, Schnabel U, Polak M, Winter J, von W Th, Brandenburg R, von dem Hagen T, Weltmann K-D (2011) Low temperature atmospheric pressure plasma sources for microbial decontamination. J Phys D 44:013002.  https://doi.org/10.1088/0022-3727/44/1/013002 CrossRefGoogle Scholar
  28. Eisenberg T, Carmona-Gutierrez D, Büttner S, Tavernarakis N, Madeo F (2010) Necrosis in yeast. Apoptosis 15(10):257–268.  https://doi.org/10.1007/s10495-009-0453-4 CrossRefPubMedGoogle Scholar
  29. Elmoualij B, Thellin O, Gofflot S, Heinen E, Levif P, Séguin J, Moisan M, Leduc A, Barbeau J, Zorzi W (2012) Decontamination of prions by the flowing afterglow of a reduced-pressure N2–O2 cold-plasma. Plasma Process Polym 9:612–618.  https://doi.org/10.1002/ppap.201100194 CrossRefGoogle Scholar
  30. Ermolaeva SA, Varfolomeev AF, Chernukha MY, Yurov DS, Vasiliev MM, Kaminskaya AA, Moisenovich MM, Romanova JM, Murashev AN, Selezneva II, Shimizu T, Sysolyatina EV, Shaginyan IA, Petrov OF, Mayevsky EI, Fortov VE, Morfil GE, Naroditsky BS, Gintsburg AL (2011) Bactericidal effects of non-thermal argon plasma in vitro, in biofilms and in the animal model of infected wounds. J Med Microbiol 60:75–83.  https://doi.org/10.1099/jmm.0.020263-0 CrossRefPubMedGoogle Scholar
  31. Eswaramoorthy N, McKenzie DR (2017) Plasma treatments of dressings for wound healing: a review. Biophys Rev 9:895–917.  https://doi.org/10.1007/s12551-017-0327-x CrossRefPubMedPubMedCentralGoogle Scholar
  32. Flynn PB, Busetti A, Wielogorska E, Chevallier OP, Elliott CT, Laverty G, Gorman SP, Graham WG, Gilmore BF (2016) Non-thermal plasma exposure rapidly attenuates bacterial AHL-dependent quorum sensing and virulence. Sci Rep 6:26320.  https://doi.org/10.1038/srep26320 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Fricke K, Koban I, Tresp H, Jablonowski L, Schrőder K, Kramer A, Weltmann KD, von Woedtke T, Kocher T (2012) Atmospheric pressure plasma: a high-performance tool for the efficient removal of biofilms. PLoS ONE 7:e42539.  https://doi.org/10.1371/journal.pone.0042539 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Fridman A, Kennedy LA (2011) Plasma physics and engineering, 2nd edn. CRC Press, Boca Raton. ISBN 9781439812280Google Scholar
  35. Fridman G, Friedman G. Gutso A, Shekhter A, Vasilets V, Fridman A (2008) Applied plasma medicine. Plasma Process Polym 5:503–533.  https://doi.org/10.1002/ppap.200700154 CrossRefGoogle Scholar
  36. Gabriel AA, Ugay M, Siringan MAT, Rosario LMD, Tumlos RB, Ramos HJ (2016) Atmospheric pressure plasma jet inactivation of Pseudomonas aeruginosa biofilms on stainless steel surfaces. Innov Food Sci Emerg Technol 36:311–319.  https://doi.org/10.1016/j.ifset.2016.07.015 CrossRefGoogle Scholar
  37. Galié S, García-Gutiérrez C, Miguélez EM, Villar CJ, Lombó F (2018) Biofilms in the food industry: health aspects and control methods. Front Microbiol 9:898.  https://doi.org/10.3389/fmicb.2018.00898 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ghafil JA (2018) Assessment the effect of non-thermal plasma on Escherichia coli and Staphylococcus aureus biofilm formtion in vitro. Iraqi J Sci 59:25–29.  https://doi.org/10.24996/ijs.2018.59.1A.4 CrossRefGoogle Scholar
  39. Gherardi M, Tonini R, Colombo V (2017) Plasma in dentistry: brief history and current status. Trends Biotechnol 36:583–585.  https://doi.org/10.1016/j.tibtech.2017.06.009 CrossRefPubMedGoogle Scholar
  40. Gilmore BF, Flynn PB, O’Brien S, Hickok N, Freeman T, Bourke P (2018) Cold plasmas for biofilm control: opportunities and challenges. Trends Biotechnol 36 538–627.  https://doi.org/10.1016/j.tibtech.2018.03.007 CrossRefGoogle Scholar
  41. Goree J, Liu B, Drake D, Stoffels E (2006) Killing of S. mutans bacteria using a plasma needle at atmospheric pressure. IEEE Trans Plasma Sci 34:1317–1324.  https://doi.org/10.1109/TPS.2006.878431 CrossRefGoogle Scholar
  42. Gorynia S, Koban I, Matthes R, Welk A, Gorynia S, Hübner N-O, Kocher T, Kramer A (2013) In vitro efficacy of cold atmospheric pressure plasma on S. sanguinis biofilms in comparison of two test models. GMS Hyg Infect Control 8:1–9.  https://doi.org/10.3205/dgkh000201 CrossRefGoogle Scholar
  43. Graves DB (2012) The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. J Phys D 45:26300.  https://doi.org/10.1088/0022-3727/45/26/263001 CrossRefGoogle Scholar
  44. Gupta TT, Karki SB, Matson JS, Gehling DJ, Ayan H (2017) Sterilization of biofilm on a titanium surface using a combination of nonthermal pasma and chlorhexidine digluconate. Biomed Res Int 2017:6085741.  https://doi.org/10.1155/2017/6085741 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Gupta TT, Karki SB, Fournier R, Ayan H (2018a) Mathematical modelling of the effects of plasma treatment on the diffusivity of biofilm. Appl Sci 8:1729.  https://doi.org/10.3390/app8101729 CrossRefGoogle Scholar
  46. Gupta TT, Matson JS, Ayan H (2018b) Antimicrobial effectiveness of regular dielectric-barrier discharge (DBD) and jet DBD on the viability of Pseudomonas aeruginosa. IEEE Trans Radiat Plasma Med Sci 2:68–76.  https://doi.org/10.1109/TPS.2017.2748982 CrossRefGoogle Scholar
  47. Gweon B, Kim K, Choe W, Shin JH (2016) Therapeutic uses of atmospheric pressure plasma: cancer and wound. In: Jo H, Jun HW, Shin J, Lee S (eds) Biomedical engineering: frontier research and converging technologies. Biosystems & biorobotics, vol 9. Springer, Cham 2016.  https://doi.org/10.1007/978-3-319-21813-7_15 CrossRefGoogle Scholar
  48. Haertel B, von Woedtke T, Weltmann K-D, Lindequist U (2014) Non-thermal atmospheric-pressure plasma: possible application in wound healing. Biomol Ther 22:477–490.  https://doi.org/10.4062/biomolther.2014.105 CrossRefGoogle Scholar
  49. Heinlin J, Morfill G, Landthaler M, Stolz W, Isbary G, Zimmermann JL, Shimizu T, Karrer S (2010) Plasma medicine: possible applications in dermatology. J German Soc Dermatol 8:968–976.  https://doi.org/10.1111/j.1610-0387.2010.07495.x CrossRefGoogle Scholar
  50. Helgadottir S, Pandit S, Mokkapati VRSS, Westerlund F, Apell P, Mijakovic I (2017) Vitamin C pretreatment enhances the antibacterial effect of cold atmospheric plasma. Front Cell Infect Microbiol 7:Article 43.  https://doi.org/10.3389/fcimb.2017.00043
  51. Hirst AM, Frame FM, Arya M, Maitland NJ, O’Connell D (2016) Low temperature plasmas as emerging cancer therapeutics: the state of play and thoughts for the future. Tumour Biol 37:7021–7031.  https://doi.org/10.1007/s13277-016-4911-7 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Hozák P, Scholtz V, Khun J, Mertová D, Vaňková E, Julák J (2018) Further contribution to the chemistry of plasma activated water: influence on bacteria in planktonic and biofilm form. Plasma Phys Rep 44:125–136.  https://doi.org/10.1134/S1063780X18010075 CrossRefGoogle Scholar
  53. Ibis F, Oflaz H, Kürsat Ercan UK (2016) Biofilm inactivation and prevention on common implant material surfaces by nonthermal DBD plasma treatment. Plasma Med 6:33–45.  https://doi.org/10.1615/PlasmaMed.2016015846 CrossRefGoogle Scholar
  54. Isbary G, Shimizu T, Li YF, Stolz W, Thomas H, Morfil G, Zimmermann JL (2013) Cold atmospheric plasma devices for medical issues. Expert Rev Med Devices 10:367–377.  https://doi.org/10.1586/erd.13.4 CrossRefPubMedGoogle Scholar
  55. Jahid IK, Han N, Ha SD (2014) Inactivation kinetics of cold oxygen plasma depend on incubation conditions of Aeromonas hydrophila biofilm on lettuce. Food Res Int 55:181–189.  https://doi.org/10.1016/j.foodres.2013.11.005 CrossRefGoogle Scholar
  56. Jiang C, Chen M-T, Gorur A, Schaudinn C, Jaramillo DE, Costerton JW, Sedghizadeh PP, Vernier PT, Gundersen MA (2009) Nanosecond pulsed plasma dental probe. Plasma Process Polym 6:479–483.  https://doi.org/10.1002/ppap.200800133 CrossRefGoogle Scholar
  57. Joubert V, Cheype C, Bonnet J, Packan D, Garnier J-P, Teissié J, Blanckaer V (2013) Inactivation of Bacillus subtilis var. niger of both spore and vegetative forms by means of corona discharges applied in water. Water Res 47:1381–1389.  https://doi.org/10.1016/j.watres.2012.12.011 CrossRefPubMedGoogle Scholar
  58. Julák J, Bednář M, Mára M (1991) Possibilities of evidence of microbial corrosion of buried pipelines (in Czech). Plyn 71:138–141Google Scholar
  59. Julák J, Janoušková O, Scholtz V, Holada K (2011) Inactivation of prions using electrical DC discharges at atmospheric pressure and ambient temperature. Plasma Process Polym 8:316–323.  https://doi.org/10.1002/ppap.201000100 CrossRefGoogle Scholar
  60. Julák J, Scholtz V, Kotúčová S, Janoušková O (2012a) The persistent microbicidal effect in water exposed to the corona discharge. Physica Med 28:230–239.  https://doi.org/10.1016/j.ejmp.2011.08.001 CrossRefGoogle Scholar
  61. Julák J, Scholtz V, Kvasničková E, Kříha V, Jíra J (2012b) Bactericidal properties of cometary discharge with inserted grid. In: Mikikian M, Rabat H, Robert E, Pouvesle J-M (eds) Book of abstracts, 4th international conference on plasma medicine, P77, p. 141, International Society for Plasma Medicine, Orléans. ICPM4-COUV-05/2012-LJGoogle Scholar
  62. Julák J, Hujacová A, Scholtz V, Khun J, Holada K (2018) Contribution to the chemistry of plasma activated water. Plasma Phys Rep 44:125–136.  https://doi.org/10.1134/S1063780X18010075 CrossRefGoogle Scholar
  63. Keidar M, Yan D, Beilis II, Trink B, Sherman JH (2017) Plasmas for treating cancer: opportunities for adaptive and self-adaptive approaches. Trends Biotechnol 36:586–593.  https://doi.org/10.1016/j.tibtech.2017.06.013 CrossRefPubMedGoogle Scholar
  64. Kelly S, Turner MM (2013) Atomic oxygen patterning from a biomedical needle-plasma source. J Appl Phys 114:123301.  https://doi.org/10.1063/1.4821241 CrossRefGoogle Scholar
  65. Khan MSI, Lee E-J, Kim Y-J (2016) A submerged dielectric barrier discharge plasma inactivation mechanism of biofilms produced by Escherichia coli O157:H7, Cronobacter sakazakii, and Staphylococcus aureus. Sci Rep 6:37072.  https://doi.org/10.1038/srep37072 CrossRefPubMedCentralGoogle Scholar
  66. Khelissa SO, Abdallah M, Jama C, Faille C, Chihib N-E (2017) Bacterial contamination and biofilm formation on abiotic surfaces and strategies to overcome their persistence. J Mater Environ Sci 8:3325–3346. HAL identifier: hal-01594685Google Scholar
  67. Khosravian N, Bogaerts A, Huygh S, Yusupov M, Neyts EC (2015) How do plasma-generated OH radicals react with biofilm components? Insights from atomic scale simulations. Biointerphases 10:029501.  https://doi.org/10.1116/1.4904339 CrossRefGoogle Scholar
  68. Khun J, Scholtz V, Hozák P, Fitl P, Julák J (2018) Various DC driven point-to-plain discharges as non-thermal plasma sources and their bactericidal effects. Plasma Sources Sci Technol 27:065002.  https://doi.org/10.1088/1361-6595/aabdd0 CrossRefGoogle Scholar
  69. Kim JH, Lee MA, Han GJ, Cho BH (2014) Plasma in dentistry: A review of basic concepts and applications in dentistry. Acta Odontol Scand 72:1–12.  https://doi.org/10.3109/00016357.2013.795660 CrossRefPubMedGoogle Scholar
  70. Klapper I, Dockery J (2010) Mathematical description of microbial biofilms. SIAM Rev 52:221–265.  https://doi.org/10.1137/080739720 CrossRefGoogle Scholar
  71. Koban I, Matthe R, Hűbner N-O, Kocher T (2010) Treatment of Candida albicans biofilms with low-temperature plasma induced by dielectric barrier discharge and atmospheric pressure plasma jet. New J Phys 12:1–16.  https://doi.org/10.1088/1367-2630/12/7/073039 CrossRefGoogle Scholar
  72. Kong MG, Kroesen G, Morfill G, Nosenko T, Shimizu T, van Dijk J, Zimmermann JL (2009) Plasma medicine: an introductory review. New J Phys 11:115012.  https://doi.org/10.1088/1367-2630/11/11/115012 CrossRefGoogle Scholar
  73. Koo H, Allan RN, Howlin RP, Stoodley P, Hall-Stoodley L (2017) Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol 15:740–755.  https://doi.org/10.1038/nrmicro.2017.99 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Kovalová Z, Tarabová K, Hensel K, Machala Z (2013) Decontamination of Streptococci biofilms and Bacillus cereus spores on plastic surfaces with DC and pulsed corona discharges. Eur Phys J Appl Phys 61:24306.  https://doi.org/10.1051/epjap/2012120449 CrossRefGoogle Scholar
  75. Kovalová Z, Zahoran M, Zahoranová A, Machala Z (2014) Streptococci biofilm decontamination on teeth by low-temperature air plasma of dc corona discharges. J Phys D: Appl Phys 47:224014.  https://doi.org/10.1088/0022-3727/47/22/224014 CrossRefGoogle Scholar
  76. Krueger AP, Smith RF, Go IG (1957) The action of air ions on bacteria. I. Protective and lethal effect on suspensions of staphylococci in droplets. J Gen Physiol 41:359–381. PMCID: PMC2194832CrossRefPubMedPubMedCentralGoogle Scholar
  77. Kumar V, Rauscher H, Brétagnol F, Arefi-Khonsar F, Pulpytel J, Colpo P, Rossi F (2010) Preventing biofilm formation on biomedical surfaces. In: Rauscher H, Perucca M, Buyle G (eds) Plasma technology for hyperfunctional surfaces: food, biomedical, and textile applications. Wiley, New York, pp. 183–223. ISBN 9783527630455,  https://doi.org/10.1002/9783527630455.ch7
  78. Kuo SP, Chen CY, Lin CS, Chiang SH (2010) Wound bleeding control by low temperature air plasma. IEEE Trans Plasma Sci 38:1908–1914.  https://doi.org/10.1109/TPS.2010.2047028 CrossRefGoogle Scholar
  79. Laroussi M, Akan T (2007) Arc-free atmospheric pressure cold plasma jets: a review. Plasma Process Polym 4:777–788.  https://doi.org/10.1002/ppap.200700066 CrossRefGoogle Scholar
  80. Laroussi M, Kong M, Morfill G, Stolz W (eds) (2012) Plasma medicine: applications of low-temperature gas plasmas in medicine and biology. Cambridge University Press, New York. ISBN 978-1-107-00643-0Google Scholar
  81. Lear G, Lewis GD (eds) (2012) Microbial biofilms: current research and applications. Caister Academic Press, Christchurch, ISBN 978-1-904455-96-7Google Scholar
  82. Lee MH, Park BJ, Jin SC, Kim D, Han I, Kim J, Hyun SO, Chung K-H, Park J-C (2009) Removal and sterilization of biofilms and planktonic bacteria by microwave-induced argon plasma at atmospheric pressure. New J Phys 11:1–11.  https://doi.org/10.1088/1367-2630/11/11/115022 CrossRefGoogle Scholar
  83. Lee HW, Nam SH, Mohamed A-AH, Kim GC, Lee JK (2010) Atmospheric pressure plasma jet composed of three electrodes: application to tooth bleaching. Plasma Process Polym 7:274–280 (2010).  https://doi.org/10.1002/ppap.200900083 CrossRefGoogle Scholar
  84. Lee HW, Park GY, Seo YS, Im YH, Shim SB, Lee HJ (2011) Modelling of atmospheric pressure plasmas for biomedical applications. J Phys D 44:053001.  https://doi.org/10.1088/0022-3727/44/5/053001 CrossRefGoogle Scholar
  85. Li Y, Sun K, Ye G, Liang Y, Pan H, Wang G, Zhao Y, Pan J, Zhang J, Fang J (2015) Evaluation of cold plasma treatment and safety in disinfecting 3-week root canal Enterococcus faecalis biofilm in vitro. J Endodont 41:1325–1330.  https://doi.org/10.1016/j.joen.2014.10.020 CrossRefGoogle Scholar
  86. Liao X, Liu D, Xiang Q, Ahn J. Chen C, Ye X, Ding T (2017) Inactivation mechanisms of non-thermal plasma on microbes: a review. Food Control 75:83–91.  https://doi.org/10.1016/j.foodcont.2016.12.021 CrossRefGoogle Scholar
  87. Lin L (2016) Prevention of biofilm formation on food contact surfaces by nanoscale plasma coatings. Thesis. Faculty of the Graduate School, University of Missouri, Columbia. https://mospace.umsystem.edu/xmlui/handle/10355/57594
  88. Liu DX, Liu ZC, Chen C, Yang AJ, Li D, Rong MZ, Chen HL, Kong MG (2016) Aqeous reactive species induced by a surface air discharge: heterogeneous mass transfer and liquid chemistry pathways. Sci Rep 6:23737.  https://doi.org/10.1038/srep23737 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Liu T, Wu L, Babu JP, Hotte TL, Garcia-Godoy F, Hong L (2017) Effects of atmospheric non-thermal argon/oxygen plasma on biofilm viability and hydrophobicity of oral bacteria. Am J Dent 30:52–56 (2017). PMID: 29178715PubMedGoogle Scholar
  90. Lloyd G, Friedman G, Jafr S, Schultz G, Fridman A, Harding K (2010) Gas plasma: Medical uses and developments in wound care. Plasma Process Polym 7:194–211.  https://doi.org/10.1002/ppap.200900097 CrossRefGoogle Scholar
  91. Lu P, Ziuzina D, Cullen PJ, Bourke P (2018) Inner surface biofilm inactivation by atmospheric pressure helium porous plasma jet. Plasma Process Polym.  https://doi.org/10.1002/ppap.201800055 CrossRefGoogle Scholar
  92. Lukeš P, Doležalová E, Sisrová I, Člupek M (2014) Aqueous-phase chemistry and bactericidal effects from an air discharge plasma in contact with water: evidence for the formation of peroxynitrite through a pseudo-second-order post-discharge reaction of H2O2 and HNO2. Plasma Sources Sci Technol 23:015019.  https://doi.org/10.1088/0963-0252/23/1/015019 CrossRefGoogle Scholar
  93. Lunov O, Zablotskii V, Churpita O, Jäger A, Polívka L, Syková E, Dejneka A, Kubinová, Š (2016) The interplay between biological and physical scenarios of bacterial death induced by non-thermal plasma. Biomaterials 82:71–83.  https://doi.org/10.1016/j.biomaterials.2015.12.027 CrossRefPubMedGoogle Scholar
  94. Machala Z, Chládeková L, Pelach M (2010) Plasma agents in bio-decontamination by dc discharges in atmospheric air. J Phys D 43:222001.  https://doi.org/10.1088/0022-3727/43/22/222001 CrossRefGoogle Scholar
  95. Machala Z, Tarabová B, Hensel K, Špetlíková E, Šikurová L, Lukeš P (2013) Formation of ROS and RNS in water electro-sprayed through transient spark discharge in air and their bactericidal effects. Plasma Process Polym 10:649–659.  https://doi.org/10.1002/ppap.201200113 CrossRefGoogle Scholar
  96. Madeo F, Fröhlich E, Fröhlich KU (1997) A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139:729–734. PMID: 9348289CrossRefPubMedPubMedCentralGoogle Scholar
  97. Madeo F, Engelhardt S, Herker E, Lehmann N, Maldene C, Proksch A, Wissing S, Fröhlich KU (2002) Apoptosis in yeast: a new model system with applications in cell biology and medicine. Curr Genet 41:208–216 (2002).  https://doi.org/10.1007/s00294-002-0310-2 CrossRefPubMedGoogle Scholar
  98. Madeo F, Herker E, Wissing S, Jungwirth H, Eisenberg T, Fröhlich KU (2004) Apoptosis in yeast. Curr Opin Microbiol 7:655–660.  https://doi.org/10.1016/j.mib.2004.10.012 CrossRefPubMedGoogle Scholar
  99. Mai-Prochnow A, Bradbury M, Ostrikov K, Murphy AB (2015) Pseudomonas aeruginosa biofilm response and resistance to cold atmospheric pressure plasma is linked to the redox-active molecule phenazine. PLoS ONE 10:e0130373.  https://doi.org/10.1371/journal.pone.0130373 CrossRefPubMedPubMedCentralGoogle Scholar
  100. Matos AO, Ricomini-Filho AP, Beline T, Ogawa ES, Oliveira BEC, Rangel EC, Da Cruz NC, Sukotjo C, Mathew MT, Barão VAR (2016) Multispecies biofilm onto plasma-treated titanium surface for dental applications. Dent Mater 32S:e40.  https://doi.org/10.1016/j.dental.2016.08.082 CrossRefGoogle Scholar
  101. Matos AO, Ricomini-Filho AP, Beline T, Ogawa ES, Costa-Oliveira BE, de Almeida AB, Nociti Junio FH, Rangel EC, da Cruz NC, Sukotjo C, Mathew MT, Barão VAR (2017) Three-species biofilm model onto plasma-treated titanium implant surface. Colloids Surf B 152:354–366.  https://doi.org/10.1016/j.colsurfb.2017.01.035 CrossRefGoogle Scholar
  102. Matthes R, Koban I, Bender C, Masur K, Kindel E, Weltmann K-D, Kocher T, Kramer A, Hűbner N-O (2013) Antimicrobial efficacy of an atmospheric pressure plasma jet against biofilms of Pseudomonas aeruginosa and Staphylococcus epidermidis. Plasma Process Polym 10:161–166.  https://doi.org/10.1002/ppap.201100133 CrossRefGoogle Scholar
  103. Matthes R, Hübner N-O, Bender C, Koban I, Horn S, Bekeschus S, Weltmann K-D, Kocher T, Kramer A, Assadian O (2014a) Efficacy of different carrier gases for barrier discharge plasma generation compared to chlorhexidine on the survival of Pseudomonas aeruginosa embedded in biofilm in vitro. Skin Pharmacol Physiol 27:148–157.  https://doi.org/10.1159/000353861 CrossRefPubMedGoogle Scholar
  104. Matthes R, Assadian O, Krame A (2014b) Repeated applications of cold atmospheric pressure plasma does not induce resistance in Staphylococcus aureus embedded in biofilms. GMS Hyg Infect Control 9:1–5.  https://doi.org/10.3205/dgkh000237 CrossRefGoogle Scholar
  105. Mercier-Bonin M, Saulou C, Lebleu N, Schmitz P, Allion A, Zanna S, Marcus P. Raynaud P, Despax B (2010) Plasma-surface engineering for biofilm prevention: evaluation of anti-adhesive and antimicrobial properties of a silver-nanocomposite thin film. In: Bailey WC (ed) Biofilms: formation, development and properties. Nova Science Publishers, Hauppauge, pp. 419–440. ISBN 978-1-61728-812-8Google Scholar
  106. Michl TD, Coad BR, Hűsler A, Valentin JDP, Vasilev K, Griesser HJ (2016) Effects of precursor and deposition conditions on prevention of bacterial biofilm growth on chlorinated plasma polymers. Plasma Process Polym 13:654–662.  https://doi.org/10.1002/ppap.201500191 CrossRefGoogle Scholar
  107. Miller V, Lin A, Fridman A (2016) Why target immune cells for plasma treatment of cancer. Plasma Chem Plasma Process 36:259–268.  https://doi.org/10.1007/s11090-015-9676-z CrossRefGoogle Scholar
  108. Mizuno A, Hori Y (1988) Destruction of living cells by pulsed high-voltage application. IEEE Trans Ind Appl 24:387–394.  https://doi.org/10.1109/28.2886 CrossRefGoogle Scholar
  109. Moisan M, Barbeau J, Moreau S, Pelletier J, Tabrizian M, Yahia L (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.  https://doi.org/10.1016/S0378-5173(01)00752-9 CrossRefPubMedGoogle Scholar
  110. Moreau M, Orange N, Feuilloley MGJ (2008) Non-thermal plasma technologies: New tools for bio-decontamination. Biotechnol Adv 26:610–617.  https://doi.org/10.1016/j.biotechadv.2008.08.001 CrossRefPubMedGoogle Scholar
  111. Morent R, De Geyter N (2011) Inactivation of bacteria by non-thermal plasmas. In: Fazel-Rezai R (ed) Biomedical engineering—frontiers and challenges. InTech, pp. 25–54.  https://doi.org/10.5772/18610
  112. Nehra V, Kumar A. Dwivedi HK (2008) Atmospheric non-thermal plasma sources. Int J Eng 2:53–68Google Scholar
  113. Nishime TMC, Borges AC, Koga-Ito CY, Machida M, Heina LRO, Kostov KG (2017) Non-thermal atmospheric pressure plasma jet applied to inactivation of different microorganisms. Surf Coat Technol 312:19–24.  https://doi.org/10.1016/j.surfcoat.2016.07.07 CrossRefGoogle Scholar
  114. Nosenko T, Shimizu T, Morfill GE (2009) Designing plasmas for chronic wound disinfection. New J Phys 11:115013.  https://doi.org/10.1088/1367-2630/11/11/115013 CrossRefGoogle Scholar
  115. Oehmigen K, Hähnel M, Brandenburg R, Wilke C, Weltmann K-D, von Woedtke T (2010) The role of acidification for antimicrobial activity of atmospheric pressure plasma in liquids. Plasma Process Polym 7:250–257.  https://doi.org/10.1002/ppap.200900077 CrossRefGoogle Scholar
  116. Oehmigen K, Winter J, Hähnel M, Wilke Ch, Brandenburg R, Weltmann K-D, von Woedtke T (2011) Estimation of possible mechanisms of escherichia coli inactivation by plasma treated sodium chloride solution. Plasma Process Polym 8:904–913.  https://doi.org/10.1002/ppap.201000099 CrossRefGoogle Scholar
  117. Pan J, Sun K, Liang Y, Sun P, Yang X, Wang J, Zhang J, Zhu W, Fang J, Becker KH (2013) Cold plasma therapy of a tooth root canal infected with Enterococcus faecalis biofilms in vitro. J Endod 39:105–110.  https://doi.org/10.1016/j.joen.2012.08.017 CrossRefPubMedGoogle Scholar
  118. Pankaj SK, Keener KM (2017) Cold plasma: background, applications and current trends. Curr Opin Food Sci 6:49–52.  https://doi.org/10.1016/j.cofs.2017.07.008 CrossRefGoogle Scholar
  119. Park JY, Park S, Choe W, Yong HI, Jo C, Kim K (2017) Plasma-functionalized solution: a potent antimicrobial agent for biomedical applications from antibacterial therapeutics to biomaterial surface engineering. ACS Appl Mater Interfaces 9:43470–43477.  https://doi.org/10.1021/acsami.7b14276 CrossRefPubMedGoogle Scholar
  120. Patange A, Boehm D, Giltrap M, Lua P, Cullen PJ, Bourke P (2018) Assessment of the disinfection capacity and eco-toxicological impact of atmospheric cold plasma for treatment of food industry effluents. Sci Total Environ 631/632:298–307.  https://doi.org/10.1016/j.scitotenv.2018.02.269 CrossRefGoogle Scholar
  121. Pavlovich MJ, Sakiyama Y, Clark DS, Graves DB (2013) Antimicrobial synergy between ambient-gas plasma and UVA treatment of aqueous solution. Plasma Process Polym 10:1051–1060.  https://doi.org/10.1002/ppap.201300065 CrossRefGoogle Scholar
  122. Pavlovich MJ, Clark DS, Graves DB (2014) Quantification of air plasma chemistry for surface disinfection. Plasma Sources Sci Technol 23:065036.  https://doi.org/10.1088/0963-0252/23/6/065036 CrossRefGoogle Scholar
  123. Pei X, Lu X. Liu., Liu D, Yang Y, Ostrikov K, Chu PK, Pan Y (2015) Inactivation of a 25.5 µm Enterococcus faecalis biofilm by a room-temperature, battery-operated, handheld air plasma jet. J Phys D 45:165205.  https://doi.org/10.1088/0022-3727/45/16/165205 CrossRefGoogle Scholar
  124. Poor AE, Ercan UK, Yost A, Brooks AD, Joshi SG (2014) Control of multi-drug-resistant pathogens with non-thermal-plasma-treated alginate wound dressing. Surg Infect 15:233–243.  https://doi.org/10.1089/sur.2013.050 CrossRefGoogle Scholar
  125. Puligundla P, Mok C (2017) Potential applications of nonthermal plasmas against biofilm-associated micro-organisms in vitro. J Appl Microbiol 122:1134–1148.  https://doi.org/10.1111/jam.13404 CrossRefPubMedGoogle Scholar
  126. Puligundla P, Mok C (2018) Inactivation of spores by nonthermal plasmas. World J Microbiol Biotechnol 34:143–155.  https://doi.org/10.1007/s11274-018-2527-3 CrossRefPubMedGoogle Scholar
  127. Rulík M, Holá V, Růžička F, Votava M (eds) (2011) Bacterial biofilms (in Czech). Univerzita Palackého, Olomouc. ISBN 978-80-2747-8Google Scholar
  128. Rupf S, Lehmann A, Hannig M, Schäfer B, Schubert A, Feldmann U, Schindler A (2010) Killing of adherent oral microbes by a non-thermal atmospheric plasma jet. J Med Microbiol 59:206–212.  https://doi.org/10.1099/jmm.0.013714-0 CrossRefPubMedGoogle Scholar
  129. Rupf S, Idlibi AN, Umanskaya N, Hannig M, Nothdurft F, Lehmann A, Schindler A, von Müller L, Spitzer W (2012) Disinfection and removal of biofilms on microstructured titanium by cold atmospheric plasma. Z Zahnärztl Impl 28:126–137.  https://doi.org/10.3238/ZZI.2012.0126-0137 CrossRefGoogle Scholar
  130. Sarji A, Tan SM, Dykes GA (2015) Surface modification of materials to encourage beneficial biofilm formation. AIMS Bioengineering 2:404–422. 0.3934/bioeng.2015.4.404CrossRefGoogle Scholar
  131. Schaudinn C, Jaramillo D, Freire MO, Sedghizadeh PP, Nguyen A, Webster P, Costerton W, Jiang C (2013) Evaluation of a nonthermal plasma needle to eliminate ex vivo biofilms in root canals of extracted human teeth. Int Endod J 46:930–937.  https://doi.org/10.1111/iej.12083 CrossRefPubMedPubMedCentralGoogle Scholar
  132. Schlege J, Köritzer J, Boxhammer V (2013) Plasma in cancer treatment. Clin Plasma Med 1:2–7.  https://doi.org/10.1016/j.cpme.2013.08.001 CrossRefGoogle Scholar
  133. Schneider S, Lackmann J-W, Ellerweg D, Denis B, Narberhaus F, Bandow JE, Benedikt J (2012) The role of VUV radiation in the inactivation of bacteria with an atmospheric pressure plasma jet. Plasma Process Polym 9:561–568.  https://doi.org/10.1002/ppap.201100102 CrossRefGoogle Scholar
  134. Scholtz V, Julák J (2010a) Plasma jet-like point-to-point electrical discharge in air and its bactericidal properties. IEEE Trans Plasma Sci 38:1978–1980.  https://doi.org/10.1109/TPS.2010.2051461 CrossRefGoogle Scholar
  135. Scholtz V, Julák J (2010b) The “cometary” discharge, a possible new type of DC electric discharge in air at atmospheric pressure, and its bactericidal properties. J Phys Conf Ser 223:012005CrossRefGoogle Scholar
  136. Scholtz V, Julák J, Kříha V (2010) The microbicidal effect of low-temperature plasma generated by corona discharge: comparison of various microorganisms on an agar surface or in aqueous suspension. Plasma Process Polym 7:237–243.  https://doi.org/10.1002/ppap.200900072 CrossRefGoogle Scholar
  137. Scholtz V, Kvasničková E, Julák J (2013) Microbial inactivation by electric discharge with metallic grid. Acta Physica Polonica A124:62–65.  https://doi.org/10.12693/APhysPolA.124.62 CrossRefGoogle Scholar
  138. Scholtz V, Soušková H, Hubka V, Švarcová M, Julák J (2015a) Inactivation of human pathogenic dermatophytes by non-thermal plasma. J Microbiol Meth 119:53–58.  https://doi.org/10.1016/j.mimet.2015.09.017 CrossRefGoogle Scholar
  139. Scholtz V, Pazlarová J, Soušková H, Khun J, Julák J (2015b) Nonthermal plasma – the tool for decontamination and disinfection. Biotechnol Adv 33:1108–1119.  https://doi.org/10.1016/j.biotechadv.2015.01.002 CrossRefPubMedGoogle Scholar
  140. Shaw A, Shama G, Iza F (2015) Emerging applications of low temperature gas plasmas in the food industry. Biointerphases 10:029402.  https://doi.org/10.1116/1.4914029 CrossRefPubMedGoogle Scholar
  141. Skariyachan S, Sridhar VS, Packirisamy S, Kumargowda ST, Challapilli SB (2018) Recent perspectives on the molecular basis of biofilm formation by Pseudomonas aeruginosa and approaches for treatment and biofilm dispersal. Folia Microbiol 63:413–432.  https://doi.org/10.1007/s12223-018-0585-4 CrossRefGoogle Scholar
  142. Sladek REJ, Filoche SK, Sissons CH, Stoffels E (2007) Treatment of Streptococcus mutans biofilms with a nonthermal atmospheric plasma. Lett Appl Microbiol 45:318–323.  https://doi.org/10.1111/j.1472-765X.2007.02194.x CrossRefPubMedGoogle Scholar
  143. Soler-Arango J, Xaubet M, Giuliani L, Grondona D, Brelles-Mariño G (2017) Air-based coaxial dielectric barrier discharge plasma source for Pseudomonas aeruginosa biofilm eradication. Plasma Medicine 7:43–63.  https://doi.org/10.1615/PlasmaMed.2017020485 CrossRefGoogle Scholar
  144. Song K, Li G, Ma Y (2014) A review on the selective apoptotic effect of nonthermal atmospheric-pressure plasma on cancer cells. Plasma Med 4:193–209.  https://doi.org/10.1615/PlasmaMed.2015012629 CrossRefGoogle Scholar
  145. Soušková H, Scholtz V, Julák J, Kommová L, Savická D, Pazlarová J (2011) The survival of micromycetes and yeasts under the low-temperature plasma generated in electrical discharge. Folia Microbiol 56:77–79.  https://doi.org/10.1007/s12223-011-0005-5 CrossRefGoogle Scholar
  146. Soušková H, Scholtz V, Julák J, Savická D (2012) The fungal spores survival under the low-temperature plasma. In: Hensel K, Machala Z, Akishev Y (eds) Plasma for bio-decontamination, medicine and food security. Springer, Dordrecht, pp. 57–66. ISBN 978-94-007-2851-6.  https://doi.org/10.1007/978-94-007-2852-3 CrossRefGoogle Scholar
  147. Sugunama R, Yasuoka K, Yasuoka T (2014) Inactivation of the biofilm by the air plasma containing water. Gaseous electronics conference 2014, American Physical Society, Abstract id. MW1.066. Bibliographic Code: 2014APS.GECMW1066SGoogle Scholar
  148. Sun Y, Yu S, Sun P, Wu H, Zhu W, Liu W, Zhang J, Fang J (2012) Inactivation of Candida biofilms by non-thermal plasma and its enhancement for fungistatic effect of antifungal drugs. PLoS ONE 7:e40629.  https://doi.org/10.1371/journal.pone.004062 CrossRefPubMedPubMedCentralGoogle Scholar
  149. Syame SM (2015) Plasma interaction with biofilm. In: The battle against microbial pathogens: basic science, technological advances and educational programs, vol. 1. Méndez-Vilas A (ed). Formatex Research Center, Badajoz, pp. 462–472. ISBN 978-84-942134-6-5Google Scholar
  150. Sysolyatina E, Mukhachev A, Yurova M, Grushin M, Karalnik V, Petryakov A, Trushkin N, Ermolaeva S. Akishev Y (2014) Role of the charged particles in bacteria inactivation by plasma of a positive and negative corona in ambient air. Plasma Process Polym 11:315–334.  https://doi.org/10.1002/ppap.201300041 CrossRefGoogle Scholar
  151. Taghizadeh L, Brackman G, Nikiforov AY, Coenye T, Leys C (2009) Antibiofilm effect of argon plasma jet. In: von Keudell A, Winter J, Böke M, Schulz-von der Gathen V (eds) Proceedings of ISPC international symposium on plasma chemistry, Bochum, 26–31. July 2009, No. 230. https://www.ispc-conference.org
  152. Taghizadeh L, Brackman G, Nikiforov A, van der Mullen J, Leys C, Coenye T (2015) Inactivation of biofilms using a low power atmospheric pressure argon plasma jet; the role of entrained nitrogen. Plasma Process Polym 12:75–78 (2015).  https://doi.org/10.1002/ppap.201400074 CrossRefGoogle Scholar
  153. Taheran L, Zarrini G, Zakerhamidi MS, Khorram S (2016) Plasma can reduce Staphylococcus epidermidis biofilm formation on medical polymers. Prog Biol Sci 6:31–36.  https://doi.org/10.22059/pbs.2016.59005 CrossRefGoogle Scholar
  154. Tendero C, Tixier C, Tristant P, Desmaison J, Leprince P (2006) Atmospheric pressure plasmas: a review. Spectrochim Acta B 61:2–30.  https://doi.org/10.1016/j.sab.2005.10.003 CrossRefGoogle Scholar
  155. Thirumdas R, Kothakota A, Annapure U, Siliveru K, Blundel R, Gatt R, Valdramidis VP (2018) Plasma activated water (PAW): chemistry, physico-chemical properties, applications in food and agriculture. Trends Food Sci Technol 77:21–31.  https://doi.org/10.1016/j.tifs.2018.05.007 CrossRefGoogle Scholar
  156. Vandervoort KG, Brelles-Mariño G (2014) Plasma-mediated inactivation of Pseudomonas aeruginosa biofilms grown on borosilicate surfaces under continuous culture system. PLoS ONE 9:e108512.  https://doi.org/10.1371/journal.pone.0108512 CrossRefPubMedPubMedCentralGoogle Scholar
  157. Vaňková E, Válková M, Scholtz V, Julák J, Khun J, Kašparová P, Masák J (2018) Prevention of biofilm redevelopment on Ti6Al4V alloy by cometary discharge with metallic grid. Contrib Plasma Phys.  https://doi.org/10.1002/ctpp.201800044 CrossRefGoogle Scholar
  158. Wu H, Moser C, Wang H-Y, Høiby N, Song ZJ (2015) Strategies for combating bacterial biofilm infections. Int J Oral Sci 7:1–7.  https://doi.org/10.1038/ijos.2014.65 CrossRefPubMedGoogle Scholar
  159. Xiong Z (2018) Cold atmospheric pressure plasmas (CAPs) for skin wound healing. In: Tutar Y (ed) Plasma medicine—concepts and clinical application. IntechOpen, Rijeka. https://www.intechopen.com/books/plasma-medicine-concepts-and-clinical-applications/cold-atmospheric-pressure-plasmas-caps-for-skin-wound-healing  https://doi.org/10.5772/intechopen.76093
  160. Xiong Z. Du T. Lu X. Cao Y. Pan Y (2011) How deep can plasma penetrate into a biofilm? Appl Phys Lett 98:221503.  https://doi.org/10.1063/1.3597622 CrossRefGoogle Scholar
  161. Xu Z, Shen J, Cheng C, Hu S, Lan Y, Chu PK (2017) In vitro antimicrobial effects and mechanism of atmospheric-pressure He/O2 plasma jet on Staphylococcus aureus biofilm. J Phys D 50:105201.  https://doi.org/10.1088/1361-6463/aa593f CrossRefGoogle Scholar
  162. Yan D, Talbot AN, Cheng ShermanH, Keidar X M (2015) Toward understanding the selective anticancer capacity of cold atmospheric plasma—a model based on aquaporins (Review). Biointerphases 10:040801.  https://doi.org/10.1116/1.4938020 CrossRefPubMedGoogle Scholar
  163. Yick S, Mai-Prochnow A, Levchenko I, Fang J, Bull MK, Bradbury M, Murphy AB, Ostrikov K (2015) The effects of plasma treatment on bacterial biofilm formation on vertically-aligned carbon nanotube arrays. RSC Adv 5:5142–5148.  https://doi.org/10.1039/c4ra08187k CrossRefGoogle Scholar
  164. Yousfi M, Merbahi N, Sarrette JP, Eichwald O, Ricard A, Gardou JP, Ducasse O, Benhenni M (2011) Non thermal plasma sources of production of active species for biomedical uses: analyses, optimization and prospect. In: Fazel-Rezai R (ed) Biomedical engineering—frontiers and challenges. InTech, pp 99–124.  https://doi.org/10.5772/19129
  165. Zelaya AJ, Stough G, Rad N, Vandervoor K, Brelles-Mariño G (2010) Pseudomonas aeruginosa biofilm inactivation: decreased cell culturability, adhesiveness to surfaces, and biofilm thickness upon high-pressure nonthermal plasma treatment. IEEE Trans Plasma Sci 38:3398–3403.  https://doi.org/10.1109/TPS.2010.2082570 CrossRefGoogle Scholar
  166. Zelaya A, Vandervoort K, Brelles-Mariño G (2012) Battling bacterial biofilms with gas discharge plasma. In: Machala Z, Hensel K, Akishev Y (eds) NATO science for peace and security series a: chemistry and biology. Springer, New York.  https://doi.org/10.1007/978-94-007-2852-3_11 CrossRefGoogle Scholar
  167. Ziuzina D, Patil S, Cullen P, Boehm D, Bourke P (2014) Dielectric barrier discharge atmospheric cold plasma for inactivation of Pseudomonas aeruginosa biofilms. Plasma Med 4:137–152.  https://doi.org/10.1615/PlasmaMed.2014011996 CrossRefGoogle Scholar
  168. Ziuzina D, Han L, Cullen PJ, Bourke P (2015a) Cold plasma inactivation of internalised bacteria and biofilms for Salmonella enterica serovar Typhimurium, Listeria monocytogenes and Escherichia coli. Int J Food Microbiol 210:53–61.  https://doi.org/10.1016/j.ijfoodmicro.2015.05.019 CrossRefPubMedGoogle Scholar
  169. Ziuzina D, Boehm D, Patil S, Cullen PJ, Bourke P (2015b) Cold plasma inactivation of bacterial biofilms and reduction of quorum sensing regulated virulence factors. PLoS ONE 10:e0138209.  https://doi.org/10.1371/journal.pone.0138209 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Institute of Immunology and Microbiology, First Faculty of MedicineCharles University and General University HospitalPrague 2Czech Republic
  2. 2.Department of Physics and MeasurementsUniversity of Chemistry and TechnologyPrague 6Czech Republic
  3. 3.Department of BiotechnologyUniversity of Chemistry and TechnologyPrague 6Czech Republic

Personalised recommendations