Abstract
The emergence and spread of antimicrobial resistance have led to a dire need for innovative, alternative intervention strategies for infectious diseases, such as cold plasma technology. Plasma, known as the “fourth state of matter,” is a reactive mix of excited and fragmented gas molecules, ions, free electrons and radicals. Cold plasma is generated by a strong electric field ionising a gas and can be applied safely onto human tissue. Early studies at the turn of the century showed cold plasma has antimicrobial activity towards several types of bacteria and fungi, ushering in plasma medicine as a potential strategy to prevent and treat infections without using antimicrobial drugs. As a result, medical plasma devices have been developed for first applications in wound care and dentistry. However, these plasma devices have only passed through small, randomised controlled trials in diabetic foot ulcers and chronic leg ulcers, while dental applications of plasma devices are limited to in vitro and ex vivo experiments. These early studies showed promising results, thereby opening new avenues of plasma technology for medical therapies. This book chapter summarises the current state of knowledge concerning how plasma medicine could revolutionise biofilm infection control.
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References
Abdo A, Schmitt-John T, Richter K (2021) Plasma-activated water as a new weapon against multidrug-resistant bacteria. EMJ Microbiol Infect Dis 2(1):38–39. ECCMID 2021 Abstract Review No. AR9
Abonti TR, Kaku M, Kojima S, Sumi H, Kojima S, Yamamoto T, Yashima Y, Miyahara H, Okino A, Kawata T, Tanne K, Tanimoto K (2016) Irradiation effects of low temperature multi gas plasma jet on oral bacteria. Dent Mater J 35(5):822–828. https://doi.org/10.4012/dmj.2016-062
Aboubakr HA, Gangal U, Youssef MM, Goyal SM, Bruggeman PJ (2016) Inactivation of virus in solution by cold atmospheric pressure plasma: identification of chemical inactivation pathways. J Phys D Appl Phys 49(20). https://doi.org/10.1088/0022-3727/49/20/204001
Alkawareek MY, Algwari QT, Gorman SP, Graham WG, O'Connell D, Gilmore BF (2012) Application of atmospheric pressure nonthermal plasma for the in vitro eradication of bacterial biofilms. FEMS Immunol Med Microbiol 65(2):381–384. https://doi.org/10.1111/j.1574-695X.2012.00942.x
Armand A, Khani M, Asnaashari M, AliAhmadi A, Shokri B (2019) Comparison study of root canal disinfection by cold plasma jet and photodynamic therapy. Photodiagnosis Photodyn Ther 26:327–333. https://doi.org/10.1016/j.pdpdt.2019.04.023
Arndt S, Landthaler M, Zimmermann JL, Unger P, Wacker E, Shimizu T, Li YF, Morfill GE, Bosserhoff AK, Karrer S (2015) Effects of cold atmospheric plasma (CAP) on ß-defensins, inflammatory cytokines, and apoptosis-related molecules in keratinocytes in vitro and in vivo. PLoS One 10(3):e0120041. https://doi.org/10.1371/journal.pone.0120041
Arndt S, Schmidt A, Karrer S, von Woedtke T (2018a) Comparing two different plasma devices kINPen and Adtec SteriPlas regarding their molecular and cellular effects on wound healing. Clin Plasma Med 9:24–33. https://doi.org/10.1016/j.cpme.2018.01.002
Arndt S, Unger P, Berneburg M, Bosserhoff AK, Karrer S (2018b) Cold atmospheric plasma (CAP) activates angiogenesis-related molecules in skin keratinocytes, fibroblasts and endothelial cells and improves wound angiogenesis in an autocrine and paracrine mode. J Dermatol Sci 89(2):181–190. https://doi.org/10.1016/j.jdermsci.2017.11.008
Azzariti A, Iacobazzi RM, Di Fonte R, Porcelli L, Gristina R, Favia P, Fracassi F, Trizio I, Silvestris N, Guida G, Tommasi S, Sardella E (2019) Plasma-activated medium triggers cell death and the presentation of immune activating danger signals in melanoma and pancreatic cancer cells. Sci Rep 9(1):4099. https://doi.org/10.1038/s41598-019-40637-z
Bakker K, Apelqvist J, Lipsky BA, Van Netten JJ, International Working Group on the Diabetic Foot (2016) The 2015 IWGDF guidance documents on prevention and management of foot problems in diabetes: development of an evidence-based global consensus. Diabetes Metab Res Rev 32(Suppl 1):2–6. https://doi.org/10.1002/dmrr.2694
Balan GG, Rosca I, Ursu EL, Doroftei F, Bostanaru AC, Hnatiuc E, Nastasa V, Sandru V, Stefanescu G, Trifan A, Mares M (2018) Plasma-activated water: a new and effective alternative for duodenoscope reprocessing. Infect Drug Resist 11:727–733. https://doi.org/10.2147/IDR.S159243
Ballout H, Hertel M, Doehring J, Kostka E, Hartwig S, Paris S, Preissner S (2018) Effects of plasma jet, dielectric barrier discharge, photodynamic therapy and sodium hypochlorite on infected curved root canals. J Biophotonics 11(3). https://doi.org/10.1002/jbio.201700186
Bernhardt T, Semmler ML, Schafer M, Bekeschus S, Emmert S, Boeckmann L (2019) Plasma medicine: Applications of cold atmospheric pressure plasma in dermatology. Oxid Med Cell Longev 2019:3873928. https://doi.org/10.1155/2019/3873928
Birmingham JG (2004) Mechanisms of bacterial spore deactivation using ambient pressure nonthermal discharges. IEEE Trans Plasma Sci 32(4):1526–1531. https://doi.org/10.1109/tps.2004.832609
Blumhagen A, Singh P, Mustapha A, Chen M, Wang Y, Yu QS (2014) Plasma deactivation of oral bacteria seeded on hydroxyapatite disks as tooth enamel analogue. Am J Dent 27(2):84–90
Borges AC, Lima GMG, Nishime TMC, Gontijo AVL, Kostov KG, Koga-Ito CY (2018) Amplitude-modulated cold atmospheric pressure plasma jet for treatment of oral candidiasis: In vivo study. PLoS One 13(6):e0199832. https://doi.org/10.1371/journal.pone.0199832
Borges AC, Kostov KG, Pessoa RS, de Abreu GMA, Lima GMG, Figueira LW, Koga-Ito CY (2021) Applications of cold atmospheric pressure plasma in dentistry. Appl Sci 11(5). https://doi.org/10.3390/app11051975
Boudam MK, Moisan M, Saoudi B, Popovici C, Gherardi N, 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 Appl Phys 39(16):3494–3507. https://doi.org/10.1088/0022-3727/39/16/s07
Brehmer F, Haenssle HA, Daeschlein G, Ahmed R, Pfeiffer S, Gorlitz A, Simon D, Schon MP, Wandke D, Emmert S (2015) Alleviation of chronic venous leg ulcers with a hand-held dielectric barrier discharge plasma generator (PlasmaDerm((R)) VU-2010): results of a monocentric, two-armed, open, prospective, randomized and controlled trial (NCT01415622). J Eur Acad Dermatol Venerol 29(1):148–155. https://doi.org/10.1111/jdv.12490
Bruggeman PJ, Iza F, Brandenburg R (2017) Foundations of atmospheric pressure non-equilibrium plasmas. Plasma Sources Sci Technol 26(12). https://doi.org/10.1088/1361-6595/aa97af
Brun P, Bernabe G, Marchiori C, Scarpa M, Zuin M, Cavazzana R, Zaniol B, Martines E (2018) Antibacterial efficacy and mechanisms of action of low power atmospheric pressure cold plasma: membrane permeability, biofilm penetration and antimicrobial sensitization. J Appl Microbiol 125(2):398–408. https://doi.org/10.1111/jam.13780
Cahill OJ, Claro T, O'Connor N, Cafolla AA, Stevens NT, Daniels S, Humphreys H (2014) Cold air plasma to decontaminate inanimate surfaces of the hospital environment. Appl Environ Microbiol 80(6):2004–2010. https://doi.org/10.1128/AEM.03480-13
Carpenter AW, Schoenfisch MH (2012) Nitric oxide release: part II. Ther Appl Chem Soc Rev 41(10):3742–3752. https://doi.org/10.1039/c2cs15273h
Carreiro AFP, Delben JA, Guedes S, Silveira EJD, Janal MN, Vergani CE, Pushalkar S, Duarte S (2019) Low-temperature plasma on peri-implant-related biofilm and gingival tissue. J Periodontol 90(5):507–515. https://doi.org/10.1002/JPER.18-0366
Caufield PW, Schon CN, Saraithong P, Li Y, Argimon S (2015) Oral Lactobacilli and dental caries: A model for niche adaptation in humans. J Dent Res 94(9 Suppl):110S–118S. https://doi.org/10.1177/0022034515576052
Cheng J-H, Lv X, Pan Y, Sun D-W (2020) Foodborne bacterial stress responses to exogenous reactive oxygen species (ROS) induced by cold plasma treatments. Trends Food Sci Technol 103:239–247. https://doi.org/10.1016/j.tifs.2020.07.022
Chuangsuwanich A, Assadamongkol T, Boonyawan D (2016) The healing effect of low-temperature atmospheric-pressure plasma in pressure ulcer: A randomized controlled trial. Int J Low Extrem Wounds 15(4):313–319. https://doi.org/10.1177/1534734616665046
Claro T, Cahill OJ, O'Connor N, Daniels S, Humphreys H (2015) Cold-air atmospheric pressure plasma against Clostridium difficile spores: a potential alternative for the decontamination of hospital inanimate surfaces. Infect Control Hosp Epidemiol 36(6):742–744. https://doi.org/10.1017/ice.2015.39
Collet G, Robert E, Lenoir A, Vandamme M, Darny T, Dozias S, Kieda C, Pouvesle JM (2014) Plasma jet-induced tissue oxygenation: potentialities for new therapeutic strategies. Plasma Sources Sci Technol 23(1). https://doi.org/10.1088/0963-0252/23/1/012005
Daeschlein G, Scholz S, Ahmed R, von Woedtke T, Haase H, Niggemeier M, Kindel E, Brandenburg R, Weltmann KD, Juenger M (2012) Skin decontamination by low-temperature atmospheric pressure plasma jet and dielectric barrier discharge plasma. J Hosp Infect 81(3):177–183. https://doi.org/10.1016/j.jhin.2012.02.012
Daeschlein G, Napp M, von Podewils S, Lutze S, Emmert S, Lange A, Klare I, Haase H, Gümbel D, von Woedtke T, Jünger M (2014) In vitro susceptibility of multidrug resistant skin and wound pathogens against low temperature atmospheric pressure plasma jet (APPJ) and dielectric barrier discharge plasma (DBD). Plasma Processes Polym 11(2):175–183. https://doi.org/10.1002/ppap.201300070
Daryabor G, Atashzar MR, Kabelitz D, Meri S, Kalantar K (2020) The effects of type 2 diabetes mellitus on organ metabolism and the immune system. Front Immunol 11:1582. https://doi.org/10.3389/fimmu.2020.01582
Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74(3):417–433. https://doi.org/10.1128/MMBR.00016-10
de la Fuente-Nunez C, Reffuveille F, Fernandez L, Hancock RE (2013) Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol 16(5):580–589. https://doi.org/10.1016/j.mib.2013.06.013
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(5):e0155427. https://doi.org/10.1371/journal.pone.0155427
Dobrynin D, Fridman G, Friedman G, Fridman A (2009) Physical and biological mechanisms of direct plasma interaction with living tissue. New J Phys 11(11). https://doi.org/10.1088/1367-2630/11/11/115020
Du T, Ma J, Yang P, Xiong Z, Lu X, Cao Y (2012) Evaluation of antibacterial effects by atmospheric pressure nonequilibrium plasmas against Enterococcus faecalis biofilms in vitro. J Endod 38(4):545–549. https://doi.org/10.1016/j.joen.2011.10.021
Duchesne C, Banzet S, Lataillade JJ, Rousseau A, Frescaline N (2019) Cold atmospheric plasma modulates endothelial nitric oxide synthase signalling and enhances burn wound neovascularisation. J Pathol 249(3):368–380. https://doi.org/10.1002/path.5323
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, Morfill 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(Pt 1):75–83. https://doi.org/10.1099/jmm.0.020263-0
FDA (n.d.) FDA authority over cosmetics: How cosmetics are not FDA-approved, but are FDA-regulated. https://www.fda.gov/cosmetics/cosmetics-laws-regulations/fda-authorityover-cosmetics-how-cosmetics-are-not-fda-approved-are-fda-regulated. Accessed 15 June 2021
Flynn PB, Higginbotham S, Alshraiedeh NH, Gorman SP, Graham WG, Gilmore BF (2015) Bactericidal efficacy of atmospheric pressure non-thermal plasma (APNTP) against the ESKAPE pathogens. Int J Antimicrob Agents 46(1):101–107. https://doi.org/10.1016/j.ijantimicag.2015.02.026
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
Flynn PB, Graham WG, Gilmore BF (2019) Acinetobacter baumannii biofilm biomass mediates tolerance to cold plasma. Lett Appl Microbiol 68(4):344–349. https://doi.org/10.1111/lam.13122
Fricke K, Koban I, Tresp H, Jablonowski L, Schroder 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(8):e42539. https://doi.org/10.1371/journal.pone.0042539
Fridman G, Friedman G, Gutsol A, Shekhter AB, Vasilets VN, Fridman A (2008) Applied plasma medicine. Plasma Processes Polym 5(6):503–533. https://doi.org/10.1002/ppap.200700154
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(6):627–638. https://doi.org/10.1016/j.tibtech.2018.03.007
Girard PM, Arbabian A, Fleury M, Bauville G, Puech V, Dutreix M, Sousa JS (2016) Synergistic effect of H2O2 and NO2 in cell death induced by cold atmospheric He plasma. Sci Rep 6:29098. https://doi.org/10.1038/srep29098
Govaert M, Smet C, Verheyen D, Walsh JL, Van Impe JFM (2019) Combined effect of cold atmospheric plasma and hydrogen peroxide treatment on mature Listeria monocytogenes and Salmonella typhimurium biofilms. Front Microbiol 10:2674. https://doi.org/10.3389/fmicb.2019.02674
Handorf O, Weihe T, Bekeschus S, Graf AC, Schnabel U, Riedel K, Ehlbeck J (2018) Nonthermal plasma jet treatment negatively affects the viability and structure of Candida albicans SC5314 biofilms. Appl Environ Microbiol 84(21). https://doi.org/10.1128/aem.01163-18
Hassett DJ, Ma JF, Elkins JG, McDermott TR, Ochsner UA, West SEH, Huang CT, Fredericks J, Burnett S, Stewart PS, McFeters G, Passador L, Iglewski BH (1999) Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34(5):1082–1093. https://doi.org/10.1046/j.1365-2958.1999.01672.x
Hebecker B, Naglik JR, Hube B, Jacobsen ID (2014) Pathogenicity mechanisms and host response during oral Candida albicans infections. Expert Rev Anti Infect Ther 12(7):867–879. https://doi.org/10.1586/14787210.2014.916210
Heinlin J, Zimmermann JL, Zeman F, Bunk W, Isbary G, Landthaler M, Maisch T, Monetti R, Morfill G, Shimizu T, Steinbauer J, Stolz W, Karrer S (2013) Randomized placebo-controlled human pilot study of cold atmospheric argon plasma on skin graft donor sites. Wound Repair Regen 21(6):800–807. https://doi.org/10.1111/wrr.12078
Herbst SR, Hertel M, Ballout H, Pierdzioch P, Weltmann KD, Wirtz HC, Abu-Sirhan S, Kostka E, Paris S, Preissner S (2015) Bactericidal efficacy of cold plasma at different depths of infected root canals in vitro. Open Dent J 9:486–491. https://doi.org/10.2174/1874210601509010486
Herrmann HW, Henins I, Park J, Selwyn GS (1999) Decontamination of chemical and biological warfare (CBW) agents using an atmospheric pressure plasma jet (APPJ). Phys Plasmas 6(5):2284–2289. https://doi.org/10.1063/1.873480
Hertel M, Schwill-Engelhardt J, Gerling T, Weltmann K-D, Imiolczyk SM, Hartwig S, Preissner S (2018) Antibacterial efficacy of plasma jet, dielectric barrier discharge, chlorhexidine, and silver diamine fluoride varnishes in caries lesions. Plasma Med 8(1):73–82. https://doi.org/10.1615/PlasmaMed.2018024767
Heuer K, Hoffmanns MA, Demir E, Baldus S, Volkmar CM, Rohle M, Fuchs PC, Awakowicz P, Suschek CV, Oplander C (2015) The topical use of non-thermal dielectric barrier discharge (DBD): nitric oxide related effects on human skin. Nitric Oxide 44:52–60. https://doi.org/10.1016/j.niox.2014.11.015
Hong Q, Dong X, Chen M, Sun H, Hong L, Wang Y, Li H, Yu Q (2019) An in vitro and in vivo study of plasma treatment effects on oral biofilms. J Oral Microbiol 11(1):1603524. https://doi.org/10.1080/20002297.2019.1603524
Huang WK, Weng CC, Liao JD, Wang YC, Chuang SF (2013) Capillary-tube-based micro-plasma system for disinfecting dental biofilm. Int J Radiat Biol 89(5):364–370. https://doi.org/10.3109/09553002.2013.756594
Hufner A, Steffen H, Holtfreter B, Schluter R, Duske K, Matthes R, von Woedtke T, Weltmann KD, Kocher T, Jablonowski L (2017) Effects of non-thermal atmospheric pressure plasma and sodium hypochlorite solution on Enterococcus faecalis biofilm: An investigation in extracted teeth. Plasma Processes Polym 14(3):1600064. https://doi.org/10.1002/ppap.201600064
Ikawa S, Tani A, Nakashima Y, Kitano K (2016) Physicochemical properties of bactericidal plasma-treated water. J Phys D Appl Phys 49(42):425401. https://doi.org/10.1088/0022-3727/49/42/425401
Isbary G, Morfill G, Schmidt HU, Georgi M, Ramrath K, Heinlin J, Karrer S, Landthaler M, Shimizu T, Steffes B, Bunk W, Monetti R, Zimmermann JL, Pompl R, Stolz W (2010) A first prospective randomized controlled trial to decrease bacterial load using cold atmospheric argon plasma on chronic wounds in patients. Br J Dermatol 163(1):78–82. https://doi.org/10.1111/j.1365-2133.2010.09744.x
Isbary G, Heinlin J, Shimizu T, Zimmermann JL, Morfill G, Schmidt HU, Monetti R, Steffes B, Bunk W, Li Y, Klaempfl T, Karrer S, Landthaler M, Stolz W (2012) Successful and safe use of 2 min cold atmospheric argon plasma in chronic wounds: results of a randomized controlled trial. Br J Dermatol 167(2):404–410. https://doi.org/10.1111/j.1365-2133.2012.10923.x
Isbary G, Stolz W, Shimizu T, Monetti R, Bunk W, Schmidt HU, Morfill GE, Klämpfl TG, Steffes B, Thomas HM, Heinlin J, Karrer S, Landthaler M, Zimmermann JL (2013) Cold atmospheric argon plasma treatment may accelerate wound healing in chronic wounds: Results of an open retrospective randomized controlled study in vivo. Clin Plasma Med 1(2):25–30. https://doi.org/10.1016/j.cpme.2013.06.001
Jo A, Joh HM, Chung TH, Chung JW (2020) Anticancer effects of plasma-activated medium produced by a microwave-excited atmospheric pressure argon plasma jet. Oxid Med Cell Longev 2020:4205640. https://doi.org/10.1155/2020/4205640
Joaquin JC, Kwan C, Abramzon N, Vandervoort K, Brelles-Marino G (2009) Is gas-discharge plasma a new solution to the old problem of biofilm inactivation? Microbiology 155(3):724–732. https://doi.org/10.1099/mic.0.021501-0
Joshi SG, Cooper M, Yost A, Paff M, Ercan UK, Fridman G, Friedman G, Fridman A, Brooks AD (2011) Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrob Agents Chemother 55(3):1053–1062. https://doi.org/10.1128/AAC.01002-10
Jungbauer G, Moser D, Muller S, Pfister W, Sculean A, Eick S (2021) The antimicrobial effect of cold atmospheric plasma against dental pathogens—a systematic review of in vitro studies. Antibiotics (Basel) 10(2). https://doi.org/10.3390/antibiotics10020211
Kalghatgi SU, Fridman G, Cooper M, Nagaraj G, Peddinghaus M, Balasubramanian M, Vasilets VN, Gutsol AF, Fridman A, Friedman G (2007) Mechanism of blood coagulation by nonthermal atmospheric pressure dielectric barrier discharge plasma. IEEE Trans Plasma Sci 35(5):1559–1566. https://doi.org/10.1109/tps.2007.905953
Kamgang-Youbi G, Herry JM, Meylheuc T, Brisset JL, Bellon-Fontaine MN, Doubla A, Naitali M (2009) Microbial inactivation using plasma-activated water obtained by gliding electric discharges. Lett Appl Microbiol 48(1):13–18. https://doi.org/10.1111/j.1472-765X.2008.02476.x
Kelly-Wintenberg K, Montie TC, Brickman C, Roth JR, Carr AK, Sorge K, Wadsworth LC, Tsai PPY (1998) Room temperature sterilization of surfaces and fabrics with a one atmosphere uniform glow discharge plasma. J Ind Microbiol Biotechnol 20(1):69–74. https://doi.org/10.1038/sj.jim.2900482
Kerlikowski A, Matthes R, Pink C, Steffen H, Schluter R, Holtfreter B, Weltmann KD, von Woedtke T, Kocher T, Jablonowski L (2020) Effects of cold atmospheric pressure plasma and disinfecting agents on Candida albicans in root canals of extracted human teeth. J Biophotonics 13(12):e202000221. https://doi.org/10.1002/jbio.202000221
Kieft IE, Laan EPvd, Stoffels E (2004) Electrical and optical characterization of the plasma needle. New J Phys 6:149–149. https://doi.org/10.1088/1367-2630/6/1/149
Kisch T, Helmke A, Schleusser S, Song J, Liodaki E, Stang FH, Mailaender P, Kraemer R (2016) Improvement of cutaneous microcirculation by cold atmospheric plasma (CAP): Results of a controlled, prospective cohort study. Microvasc Res 104:55–62. https://doi.org/10.1016/j.mvr.2015.12.002
Koban I, Matthes R, Hübner N-O, Welk A, Meisel P, Holtfreter B, Sietmann R, Kindel E, Weltmann K-D, Kramer A, 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(7). https://doi.org/10.1088/1367-2630/12/7/073039
Koban I, Holtfreter B, Hubner NO, Matthes R, Sietmann R, Kindel E, Weltmann KD, Welk A, Kramer A, Kocher T (2011) Antimicrobial efficacy of non-thermal plasma in comparison to chlorhexidine against dental biofilms on titanium discs in vitro - proof of principle experiment. J Clin Periodontol 38(10):956–965. https://doi.org/10.1111/j.1600-051X.2011.01740.x
Kogelheide F, Voigt F, Hillebrand B, Moeller R, Fuchs F, Gibson AR, Awakowicz P, Stapelmann K, Fiebrandt M (2020) The role of humidity and UV-C emission in the inactivation of B. subtilis spores during atmospheric-pressure dielectric barrier discharge treatment. J Phys D Appl Phys 53(29). https://doi.org/10.1088/1361-6463/ab77cc
Kondeti VSSK, Phan CQ, Wende K, Jablonowski H, Gangal U, Granick JL, Hunter RC, Bruggeman PJ (2018) 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. https://doi.org/10.1016/j.freeradbiomed.2018.05.083
Kramer B, Hasse D, Guist S, Schmitt-John T, Muranyi P (2019) Inactivation of bacterial endospores on surfaces by plasma processed air. J Appl Microbiol 128(4):920–933. https://doi.org/10.1111/jam.14528
Lamont RJ, Koo H, Hajishengallis G (2018) The oral microbiota: dynamic communities and host interactions. Nat Rev Microbiol 16(12):745–759. https://doi.org/10.1038/s41579-018-0089-x
Laroussi M (2020) Cold plasma in medicine and healthcare: The new frontier in low temperature plasma applications. Front Phys 8. https://doi.org/10.3389/fphy.2020.00074
Laroussi M, Leipold F (2004) Evaluation of the roles of reactive species, heat, and UV radiation in the inactivation of bacterial cells by air plasmas at atmospheric pressure. Int J Mass Spectrom 233(1-3):81–86. https://doi.org/10.1016/j.ijms.2003.11.016
Laurita R, Barbieri D, Gherardi M, Colombo V, Lukes P (2015) Chemical analysis of reactive species and antimicrobial activity of water treated by nanosecond pulsed DBD air plasma. Clin Plasma Med 3(2):53–61. https://doi.org/10.1016/j.cpme.2015.10.001
Lee K-Y, Joo Park B, Hee Lee D, Lee I-S, Hyun SO, Chung K-H, Park J-C (2005) Sterilization of Escherichia coli and MRSA using microwave-induced argon plasma at atmospheric pressure. Surf Coat Technol 193(1–3):35–38. https://doi.org/10.1016/j.surfcoat.2004.07.034
Lee JY, Kim KH, Park SY, Yoon SY, Kim GH, Lee YM, Rhyu IC, Seol YJ (2019) The bactericidal effect of an atmospheric-pressure plasma jet on Porphyromonas gingivalis biofilms on sandblasted and acid-etched titanium discs. J Periodontal Implant Sci 49(5):319–329. https://doi.org/10.5051/jpis.2019.49.5.319
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 Endod 41(8):1325–1330. https://doi.org/10.1016/j.joen.2014.10.020
Li Y, Pan J, Ye G, Zhang Q, Wang J, Zhang J, Fang J (2017) In vitro studies of the antimicrobial effect of non-thermal plasma-activated water as a novel mouthwash. Eur J Oral Sci 125(6):463–470. https://doi.org/10.1111/eos.12374
Li Y, Pan J, Wu D, Tian Y, Zhang J, Fang J (2019) Regulation of Enterococcus faecalis biofilm formation and quorum sensing related virulence factors with ultra-low dose reactive species produced by plasma activated water. Plasma Chem Plasma Process 39(1):35–49. https://doi.org/10.1007/s11090-018-9930-2
Lietz AM, Kushner MJ (2018) Molecular admixtures and impurities in atmospheric pressure plasma jets. J Appl Phys 124(15). https://doi.org/10.1063/1.5049430
Liguori A, Cochis A, Stancampiano A, Laurita R, Azzimonti B, Sorrentino R, Varoni EM, Petri M, Colombo V, Gherardi M, Rimondini L (2017) Cold atmospheric plasma treatment affects early bacterial adhesion and decontamination of soft reline palatal obturators. Clin Plasma Med 7–8:36–45. https://doi.org/10.1016/j.cpme.2017.08.001
Limoli DH, Jones CJ, Wozniak DJ (2015) Bacterial extracellular polysaccharides in biofilm formation and function. Microbiol Spectr 3(3). https://doi.org/10.1128/microbiolspec.MB-0011-2014
Lis KA, Kehrenberg C, Boulaaba A, von Kockritz-Blickwede M, Binder S, Li Y, Zimmermann JL, Pfeifer Y, Ahlfeld B (2018) Inactivation of multidrug-resistant pathogens and Yersinia enterocolitica with cold atmospheric-pressure plasma on stainless-steel surfaces. Int J Antimicrob Agents 52(6):811–818. https://doi.org/10.1016/j.ijantimicag.2018.08.023
Liu ZC, Liu DX, Chen C, Li D, Yang AJ, Rong MZ, Chen HL, Kong MG (2015) Physicochemical processes in the indirect interaction between surface air plasma and deionized water. J Phys D Appl Phys 48(49). https://doi.org/10.1088/0022-3727/48/49/495201
Liu K, Ren W, Ran C, Zhou R, Tang W, Zhou R, Yang Z, Ostrikov K (2021) Long-lived species in plasma-activated water generated by an AC multi-needle-to-water discharge: effects of gas flow on chemical reactions. J Phys D Appl Phys 54(6). https://doi.org/10.1088/1361-6463/abc211
Lu X, Naidis GV, Laroussi M, Reuter S, Graves DB, Ostrikov K (2016) Reactive species in non-equilibrium atmospheric-pressure plasmas: Generation, transport, and biological effects. Phys Rep 630:1–84. https://doi.org/10.1016/j.physrep.2016.03.003
Ma R, Wang G, Tian Y, Wang K, Zhang J, Fang J (2015) Non-thermal plasma-activated water inactivation of food-borne pathogen on fresh produce. J Hazard Mater 300:643–651. https://doi.org/10.1016/j.jhazmat.2015.07.061
Mai-Prochnow A, Murphy AB, McLean KM, Kong MG, Ostrikov KK (2014) Atmospheric pressure plasmas: infection control and bacterial responses. Int J Antimicrob Agents 43(6):508–517. https://doi.org/10.1016/j.ijantimicag.2014.01.025
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(6):e0130373. https://doi.org/10.1371/journal.pone.0130373
Mai-Prochnow A, Clauson M, Hong J, Murphy AB (2016) Gram positive and Gram negative bacteria differ in their sensitivity to cold plasma. Sci Rep 6:38610. https://doi.org/10.1038/srep38610
Marsh PD (2003) Are dental diseases examples of ecological catastrophes? Microbiology (Reading) 149(Pt 2):279–294. https://doi.org/10.1099/mic.0.26082-0
Marsh PD, Head DA, Devine DA (2015) Dental plaque as a biofilm and a microbial community—Implications for treatment. J Oral Biosci 57(4):185–191. https://doi.org/10.1016/j.job.2015.08.002
Matthes R, Koban I, Bender C, Masur K, Kindel E, Weltmann K-D, Kocher T, Kramer A, Hübner N-O (2013) Antimicrobial efficacy of an atmospheric pressure plasma jet against biofilms of Pseudomonas aeruginosa and Staphylococcus epidermidis. Plasma Processes Polym 10(2):161–166. https://doi.org/10.1002/ppap.201100133
Matthes R, Assadian O, Kramer A (2014) Repeated applications of cold atmospheric pressure plasma does not induce resistance in Staphylococcus aureus embedded in biofilms. GMD Hyg. Infect Control 9(3):Doc17. https://doi.org/10.3205/dgkh000237
Matthes R, Jablonowski L, Koban I, Quade A, Hubner NO, Schlueter R, Weltmann KD, von Woedtke T, Kramer A, Kocher T (2015) In vitro treatment of Candida albicans biofilms on denture base material with volume dielectric barrier discharge plasma (VDBD) compared with common chemical antiseptics. Clin Oral Investig 19:2319–2326. https://doi.org/10.1007/s00784-015-1463-y
Mirpour S, Fathollah S, Mansouri P, Larijani B, Ghoranneviss M, Mohajeri Tehrani M, Amini MR (2020) Cold atmospheric plasma as an effective method to treat diabetic foot ulcers: A randomized clinical trial. Sci Rep 10(1):10440. https://doi.org/10.1038/s41598-020-67232-x
Modic M, McLeod NP, Sutton JM, Walsh JL (2017) Cold atmospheric pressure plasma elimination of clinically important single- and mixed-species biofilms. Int J Antimicrob Agents 49(3):375–378. https://doi.org/10.1016/j.ijantimicag.2016.11.022
Molnar I, Papp J, Simon A, Anghel SD (2013) Deactivation of Streptococcus mutans biofilms on a tooth surface using He dielectric barrier discharge at atmospheric pressure. Plasma Sci Technol 15(6):535–541. https://doi.org/10.1088/1009-0630/15/6/09
Muro-Fraguas I, Sainz-Garcia A, Lopez M, Rojo-Bezares B, Mugica-Vidal R, Sainz-Garcia E, Toledano P, Saenz Y, Gonzalez-Marcos A, Alba-Elias F (2020) Antibiofilm coatings through atmospheric pressure plasma for 3D printed surgical instruments. Surf Coat Technol 399:126163. https://doi.org/10.1016/j.surfcoat.2020.126163
Naitali M, Kamgang-Youbi G, Herry JM, Bellon-Fontaine MN, Brisset JL (2010) Combined effects of long-living chemical species during microbial inactivation using atmospheric plasma-treated water. Appl Environ Microbiol 76(22):7662–7664. https://doi.org/10.1128/AEM.01615-10
Nguyen NH, Park HJ, Yang SS, Choi KS, Lee JS (2016) Anti-cancer efficacy of nonthermal plasma dissolved in a liquid, liquid plasma in heterogeneous cancer cells. Sci Rep 6:29020. https://doi.org/10.1038/srep29020
Nicol MJ, Brubaker TR, Honish BJ 2nd, Simmons AN, Kazemi A, Geissel MA, Whalen CT, Siedlecki CA, Bilen SG, Knecht SD, Kirimanjeswara GS (2020) Antibacterial effects of low-temperature plasma generated by atmospheric-pressure plasma jet are mediated by reactive oxygen species. Sci Rep 10(1):3066. https://doi.org/10.1038/s41598-020-59652-6
Noopan S, Unchui P, Techotinnakorn S, Ampornaramveth RS (2019) Plasma sterilization effectively reduces bacterial contamination in dental unit waterlines. Int J Dentist 2019:5720204. https://doi.org/10.1155/2019/5720204
Otter JA, Yezli S, French GL (2011) The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infect Control Hosp Epidemiol 32(7):687–699. https://doi.org/10.1086/660363
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(1):105–110. https://doi.org/10.1016/j.joen.2012.08.017
Pan J, Li YL, Liu CM, Tian Y, Yu S, Wang KL, Zhang J, Fang J (2017) Investigation of cold atmospheric plasma-activated water for the dental unit waterline system contamination and safety evaluation in vitro. Plasma Chem Plasma Process 37(4):1091–1103. https://doi.org/10.1007/s11090-017-9811-0
Pankaj SK, Bueno-Ferrer C, Misra NN, O'Neill L, Bourke P, Cullen PJ (2017) Effects of cold plasma on surface, thermal and antimicrobial release properties of chitosan film. J Renew Mater 5(1):14–20. https://doi.org/10.7569/jrm.2016.634105
Park JH, Kim M, Shiratani M, Cho AE, Choi EH, Attri P (2016) Variation in structure of proteins by adjusting reactive oxygen and nitrogen species generated from dielectric barrier discharge jet. Sci Rep 6:35883. https://doi.org/10.1038/srep35883
Park S, Park JY, Choe W (2019) Origin of hydroxyl radicals in a weakly ionized plasma-facing liquid. Chem Eng J 378. https://doi.org/10.1016/j.cej.2019.122163
Preissner S, Wirtz HC, Tietz AK, Abu-Sirhan S, Herbst SR, Hartwig S, Pierdzioch P, Schmidt-Westhausen AM, Dommisch H, Hertel M (2016) Bactericidal efficacy of tissue tolerable plasma on microrough titanium dental implants: An in-vitro-study. J Biophotonics 9(6):637–644. https://doi.org/10.1002/jbio.201500189
Puligundla P, Mok C (2017) Potential applications of nonthermal plasmas against biofilm-associated micro-organisms in vitro. J Appl Microbiol 122(5):1134–1148. https://doi.org/10.1111/jam.13404
Puttaiah R, Karpay RI, Fabre C, Sherman LR, Nemeth JF, Mills SE, Plamondon TJ (1998) Dental unit water line treatment with sodium hypochlorite and acetic acid. Microchem J 59(2):333–340. https://doi.org/10.1006/mchj.1998.1589
Reuter S, von Woedtke T, Weltmann KD (2018) The kINPen-a review on physics and chemistry of the atmospheric pressure plasma jet and its applications. J Phys D Appl Phys 51(233001). https://doi.org/10.1088/1361-6463/aab3ad
Rodriguez C, Wandell RJ, Zhang Z, Neurohr JM, Tang Y, Rhodes R, Kinsey ST, Locke BR (2020) Escherichia coli survival in plasma-treated water and in a gas–liquid plasma reactor. Plasma Processes Polym 17(12). https://doi.org/10.1002/ppap.202000099
Royintarat T, Seesuriyachan P, Boonyawan D, Choi EH, Wattanutchariya W (2019) Mechanism and optimization of non-thermal plasma-activated water for bacterial inactivation by underwater plasma jet and delivery of reactive species underwater by cylindrical DBD plasma. Curr Appl Phys 19(9):1006–1014. https://doi.org/10.1016/j.cap.2019.05.020
Saitaer X, Sanbhal N, Qiao Y, Li Y, Gao J, Brochu G, Guidoin R, Khatri A, Wang L (2019) Polydopamine-inspired surface modification of polypropylene hernia mesh devices via cold oxygen plasma: antibacterial and drug release properties. Coatings 9(3). https://doi.org/10.3390/coatings9030164
Salgado BAB, Fabbri S, Dickenson A, Hasan MI, Walsh JL (2021) Surface barrier discharges for Escherichia coli biofilm inactivation: Modes of action and the importance of UV radiation. PLoS One 16(3):e0247589. https://doi.org/10.1371/journal.pone.0247589
Sanbhal N, Mao Y, Sun G, Xu RF, Zhang Q, Wang L (2018a) Surface modification of polypropylene mesh devices with cyclodextrin via cold plasma for hernia repair: Characterization and antibacterial properties. Appl Surf Sci 439:749–759. https://doi.org/10.1016/j.apsusc.2017.12.192
Sanbhal N, Mao Y, Sun G, Li Y, Peerzada M, Wang L (2018b) Preparation and characterization of antibacterial polypropylene meshes with covalently incorporated beta-cyclodextrins and captured antimicrobial agent for hernia repair. Polymers (Basel) 10(1). https://doi.org/10.3390/polym10010058
Sanbhal N, Li Y, Khatri A, Peerzada M, Wang L (2019) Chitosan cross-linked bio-based antimicrobial polypropylene meshes for hernia repair loaded with levofloxacin HCl via cold oxygen plasma. Coatings 9(3). https://doi.org/10.3390/coatings9030168
Schaudinn C, Jaramillo D, Freire MO, Sedghizadeh PP, Nguyen A, Webster P, Costerton JW, 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(10):930–937. https://doi.org/10.1111/iej.12083
Schnabel U, Handorf O, Stachowiak J, Boehm D, Weit C, Weihe T, Schäfer J, Below H, Bourke P, Ehlbeck J (2020) Plasma-functionalized water: from bench to prototype for fresh-cut lettuce. Food Eng Rev 13(1):115–135. https://doi.org/10.1007/s12393-020-09238-9
Schneider S, Lackmann JW, Narberhaus F, Bandow JE, Denis B, Benedikt J (2011) Separation of VUV/UV photons and reactive particles in the effluent of a He/O2atmospheric pressure plasma jet. J Phys D Appl Phys 44(37). https://doi.org/10.1088/0022-3727/44/37/379501
Scholtz V, Pazlarova J, Souskova H, Khun J, Julak J (2015) Nonthermal plasma-A tool for decontamination and disinfection. Biotechnol Adv 33(6):1108–1119. https://doi.org/10.1016/j.biotechadv.2015.01.002
Semmler ML, Bekeschus S, Schafer M, Bernhardt T, Fischer T, Witzke K, Seebauer C, Rebl H, Grambow E, Vollmar B, Nebe JB, Metelmann HR, Woedtke TV, Emmert S, Boeckmann L (2020) Molecular mechanisms of the efficacy of cold atmospheric pressure plasma (CAP) in cancer treatment. Cancers (Basel) 12(2). https://doi.org/10.3390/cancers12020269
Sharma A, Collins G, Pruden A (2009) Differential gene expression in Escherichia coli following exposure to nonthermal atmospheric pressure plasma. J Appl Microbiol 107(5):1440–1449. https://doi.org/10.1111/j.1365-2672.2009.04323.x
Sheiham A, James WPT (2014) A reappraisal of the quantitative relationship between sugar intake and dental caries: the need for new criteria for developing goals for sugar intake. BMC Public Health 14. https://doi.org/10.1186/1471-2458-14-863
Shekhter AB, Serezhenkov VA, Rudenko TG, Pekshev AV, Vanin AF (2005) Beneficial effect of gaseous nitric oxide on the healing of skin wounds. Nitric Oxide 12(4):210–219. https://doi.org/10.1016/j.niox.2005.03.004
Shen J, Tian Y, Li Y, Ma R, Zhang Q, Zhang J, Fang J (2016) Bactericidal effects against S. aureus and physicochemical properties of plasma activated water stored at different temperatures. Sci Rep 6:28505. https://doi.org/10.1038/srep28505
Silk H (2014) Diseases of the mouth. Prim Care 41(1):75–90. https://doi.org/10.1016/j.pop.2013.10.011
Stoffels E, Kieft IE, Sladek REJ (2003) Superficial treatment of mammalian cells using plasma needle. J Phys D Appl Phys 36(23):2908–2913. https://doi.org/10.1088/0022-3727/36/23/007
Stoleru E, Dumitriu RP, Munteanu BS, Zaharescu T, Tănase EE, Mitelut A, Ailiesei G-L, Vasile C (2016) Novel procedure to enhance PLA surface properties by chitosan irreversible immobilization. Appl Surf Sci 367:407–417. https://doi.org/10.1016/j.apsusc.2016.01.200
Stratmann B, Costea TC, Nolte C, Hiller J, Schmidt J, Reindel J, Masur K, Motz W, Timm J, Kerner W, Tschoepe D (2020) Effect of cold atmospheric plasma therapy vs standard therapy placebo on wound healing in patients with diabetic foot ulcers: A randomized clinical trial. JAMA Netw Open 3(7):e2010411. https://doi.org/10.1001/jamanetworkopen.2020.10411
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 Processes Polym 12(1):75–81. https://doi.org/10.1002/ppap.201400074
Tarabova B, Lukes P, Hammer MU, Jablonowski H, von Woedtke T, Reuter S, Machala Z (2019) Fluorescence measurements of peroxynitrite/peroxynitrous acid in cold air plasma treated aqueous solutions. Phys Chem Chem Phys 21(17):8883–8896. https://doi.org/10.1039/c9cp00871c
Tendero C, Tixier C, Tristant P, Desmaison J, Leprince P (2006) Atmospheric pressure plasmas: A review. Spectrochim Acta Part B Atomic Spectrosc 61(1):2–30. https://doi.org/10.1016/j.sab.2005.10.003
Thirumdas R, Kothakota A, Annapure U, Siliveru K, Blundell 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
Tian Y, Ma R, Zhang Q, Feng H, Liang Y, Zhang J, Fang J (2015) Assessment of the physicochemical properties and biological effects of water activated by non-thermal plasma above and beneath the water surface. Plasma Processes Polym 12(5):439–449. https://doi.org/10.1002/ppap.201400082
Trompeter FJ, Neff WJ, Franken O, Heise M, Neiger M, Shuhai L, Pietsch GJ, Saveljew AB (2002) Reduction of Bacillus subtilis and Aspergillus niger spores using nonthermal atmospheric gas discharges. IEEE Trans Plasma Sci 30(4):1416–1423. https://doi.org/10.1109/tps.2002.804182
Ulrich C, Kluschke F, Patzelt A, Vandersee S, Czaika VA, Richter H, Bob A, von Hutten J, Painsi C, Hüge R, Kramer A, Assadian O, Lademann J, Lange-Asschenfeldt B (2015) Clinical use of cold atmospheric pressure argon plasma in chronic leg ulcers: A pilot study. J Wound Care 24(5):196, 198–200, 202–193. https://doi.org/10.12968/jowc.2015.24.5.196
Ureyen Kaya B, Kececi AD, Guldas HE, Cetin ES, Ozturk T, Oksuz L, Bozduman F (2014) Efficacy of endodontic applications of ozone and low-temperature atmospheric pressure plasma on root canals infected with Enterococcus faecalis. Lett Appl Microbiol 58(1):8–15. https://doi.org/10.1111/lam.12148
Vandervoort KG, Abramzon N, Brelles-Marino G (2008) Plasma interactions with bacterial biofilms as visualized through atomic force microscopy. IEEE Trans Plasma Sci 36(4):1296–1297. https://doi.org/10.1109/tps.2008.917953
von Woedtke T, Emmert S, Metelmann H-R, Rupf S, Weltmann K-D (2020) Perspectives on cold atmospheric plasma (CAP) applications in medicine. Phys Plasmas 27(7):070601. https://doi.org/10.1063/5.0008093
Wang Q, Salvi D (2021) Evaluation of plasma-activated water (PAW) as a novel disinfectant: Effectiveness on Escherichia coli and Listeria innocua, physicochemical properties, and storage stability. LWT Food Sci Technol 149. https://doi.org/10.1016/j.lwt.2021.111847
Whitehead-Clarke T, Windsor A (2021) Surgical site infection: The scourge of abdominal wall reconstruction. Surg Infect (Larchmt) 22(4):357–362. https://doi.org/10.1089/sur.2020.325
Whiteley M, Diggle SP, Greenberg EP (2017) Progress in and promise of bacterial quorum sensing research. Nature 551(7680):313–320. https://doi.org/10.1038/nature24624
Xu Z, Shen J, Zhang Z, Ma J, Ma R, Zhao Y, Sun Q, Qian S, Zhang H, Ding L, Cheng C, Chu PK, Xia W (2015) Inactivation effects of non-thermal atmospheric-pressure helium plasma jet on Staphylococcus aureus biofilms. Plasma Processes Polym 12(8):827–835. https://doi.org/10.1002/ppap.201500006
Xu Z, Zhou X, Yang W, Zhang Y, Ye Z, Hu S, Ye C, Li Y, Lan Y, Shen J, Ye X, Yang F, Cheng C (2020) In vitro antimicrobial effects and mechanism of air plasma-activated water on Staphylococcus aureus biofilm. Plasma Processes Polym 17(8). https://doi.org/10.1002/ppap.201900270
Yan DY, Sherman JH, Keidar M (2017) Cold atmospheric plasma, a novel promising anti-cancer treatment modality. Oncotarget 8(9):15977–15995. https://doi.org/10.18632/oncotarget.13304
Yang B, Chen JR, Yu QS, Li H, Lin MS, Mustapha A, Hong LA, Wang Y (2011) Oral bacterial deactivation using a low-temperature atmospheric argon plasma brush. J Dent 39(1):48–56. https://doi.org/10.1016/j.jdent.2010.10.002
Yang Y, Guo J, Zhou X, Liu Z, Wang C, Wang K, Zhang J, Wang Z (2018) A novel cold atmospheric pressure air plasma jet for peri-implantitis treatment: An in vitro study. Dent Mater J 37(1):157–166. https://doi.org/10.4012/dmj.2017-030
Zhang Q, Liang Y, Feng H, Ma R, Tian Y, Zhang J, Fang J (2013) A study of oxidative stress induced by non-thermal plasma-activated water for bacterial damage. Appl Phys Lett 102(20):203701. https://doi.org/10.1063/1.4807133
Zhang Q, Ma R, Tian Y, Su B, Wang K, Yu S, Zhang J, Fang J (2016) Sterilization efficiency of a novel electrochemical disinfectant against Staphylococcus aureus. Environ Sci Technol 50(6):3184–3192. https://doi.org/10.1021/acs.est.5b05108
Zhang X, Zhou R, Bazaka K, Liu Y, Zhou R, Chen G, Chen Z, Liu Q, Yang S, Ostrikov KK (2018) Quantification of plasma produced OH radical density for water sterilization. Plasma Processes Polym 15(6):1700241. https://doi.org/10.1002/ppap.201700241
Zhang H, Tian Y, Kang M, Chen C, Song Y, Li H (2019) Effects of chlorination/chlorine dioxide disinfection on biofilm bacterial community and corrosion process in a reclaimed water distribution system. Chemosphere 215:62–73. https://doi.org/10.1016/j.chemosphere.2018.09.181
Zhao YM, Patange A, Sun DW, Tiwari B (2020a) Plasma-activated water: Physicochemical properties, microbial inactivation mechanisms, factors influencing antimicrobial effectiveness, and applications in the food industry. Compr Rev Food Sci Food Saf 19(6):3951–3979. https://doi.org/10.1111/1541-4337.12644
Zhao YM, Ojha S, Burgess CM, Sun DW, Tiwari BK (2020b) Inactivation efficacy of plasma-activated water: influence of plasma treatment time, exposure time and bacterial species. Int J Food Sci Technol 56(2):721–732. https://doi.org/10.1111/ijfs.14708
Zhou R, Zhou R, Prasad K, Fang Z, Speight R, Bazaka K, Ostrikov K (2018) Cold atmospheric plasma activated water as a prospective disinfectant: the crucial role of peroxynitrite. Green Chem 20(23):5276–5284. https://doi.org/10.1039/c8gc02800a
Zhou R, Zhou R, Wang P, Luan B, Zhang X, Fang Z, Xian Y, Lu X, Ostrikov KK, Bazaka K (2019) Microplasma bubbles: Reactive vehicles for biofilm dispersal. ACS Appl Mater Interfaces 11(23):20660–20669. https://doi.org/10.1021/acsami.9b03961
Zhou R, Zhou R, Wang P, Xian Y, Mai-Prochnow A, Lu X, Cullen PJ, Ostrikov K, Bazaka K (2020) Plasma-activated water: generation, origin of reactive species and biological applications. J Phys D Appl Phys 53(30):303001. https://doi.org/10.1088/1361-6463/ab81cf
Zimmermann JL, Shimizu T, Schmidt HU, Li YF, Morfill GE, Isbary G (2012) Test for bacterial resistance build-up against plasma treatment. New J Phys 14(7). https://doi.org/10.1088/1367-2630/14/7/073037
Ziuzina D, Boehm D, Patil S, Cullen PJ, Bourke P (2015) Cold plasma inactivation of bacterial biofilms and reduction of quorum sensing regulated virulence factors. PLoS One 10(9):e0138209. https://doi.org/10.1371/journal.pone.0138209
Acknowledgements
Work in the laboratory and for this review was supported by the National Health and Medical Research Council (GNT1163634, GNT2004036), the University of Adelaide and The Hospital Research Foundation, Australia. The authors kindly acknowledge Animate Your Science (www.animateyour.science) for professional graphics.
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Abdo, A.I., Schmitt-John, T., Richter, K. (2022). Cold Plasma Therapy as a Physical Antibiofilm Approach. In: Richter, K., Kragh, K.N. (eds) Antibiofilm Strategies. Springer Series on Biofilms, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-031-10992-8_10
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