Cold Atmospheric Plasma as a Therapeutic Tool in Medicine and Dentistry

This comprehensive review explores decade-long research conducted on the applications of Cold Atmospheric Plasma (CAP) and Plasma Activated Liquids (PAL), including Plasma Activated Water (PAW), in the fields of Medicine and Dentistry. CAPs, operating at atmospheric pressure, offer unique advantages over conventional medical devices, generating Reactive Oxygen Species (ROS) and Reactive Nitrogen Species (RNS) that interact with substances, enabling diverse applications. The review examined CAP and PAL efficacy against infectious diseases using in vitro, ex vivo, in vivo, and direct application methods. Significant strides were observed in wound healing, cancer treatment, and dental care. However, ensuring patient safety through rigorous plasma source standards remains crucial. The study underscores CAPs and PALs’ potential to transform medical and dental therapies, urging further research and development in these groundbreaking technologies. These findings highlight the transformative impact of CAPs and PALs, offering promising avenues for innovative medical and dental treatments.

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

Access this article

Subscribe and save

Springer+ Basic €32.70 /Month

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Rent this article via DeepDyve

Similar content being viewed by others

Plasma Care®

Chapter © 2022

Cold Plasma Therapy as a Physical Antibiofilm Approach

Chapter © 2022

Technical applications of plasma treatments: current state and perspectives

Article 15 May 2019

Data Availability

References

  1. Hoffmann C, Berganza C, Zhang J (2013) Cold Atmospheric plasma: methods of production and application in dentistry and oncology. Med Gas Res 3(1):21. https://doi.org/10.1186/2045-9912-3-21PMID: 24083477; PMCID: PMC4016545 ArticlePubMedPubMed CentralGoogle Scholar
  2. Borges AC, Kostov KG, Pessoa RS, de Abreu GMA, Lima GdMG, Figueira LW, Koga-Ito CY (2021) Applications of Cold Atmospheric pressure plasma in Dentistry. Appl Sci 11:1975. https://doi.org/10.3390/app11051975ArticleCASGoogle Scholar
  3. Braný D, Dvorská D, Halašová E, Škovierová H (2020) Cold Atmospheric plasma: a powerful Tool for Modern Medicine. Int J Mol Sci 21(8):2932. https://doi.org/10.3390/ijms21082932PMID: 32331263; PMCID: PMC7215620 ArticleCASPubMedPubMed CentralGoogle Scholar
  4. Y, Dayun JH, Sherman, and Michael Keidar (2017) Cold Atmospheric plasma, a Novel Promising Anti-Cancer Treatment Modality. Oncotarget 8(9):15977–15995. https://doi.org/10.18632/oncotarget.13304
  5. Chen Z, Chen G, Obenchain R, Zhang R, Bai F, Fang T, Wang H, Lu Y, Wirz RE, Gu Z (2022) Cold atmospheric plasma delivery for biomedical applications. Mater Today 54:153–188. https://doi.org/10.1016/j.mattod.2022.03.001ArticleCASGoogle Scholar
  6. 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 ArticleGoogle Scholar
  7. Milhan NVM, Chiappim W, Sampaio AdG, Vegian MRdC, Pessoa RS, Koga-Ito CY (2022) Applications of plasma-activated water in Dentistry: a review. Int J Mol Sci 23:4131. https://doi.org/10.3390/ijms23084131ArticlePubMedPubMed CentralGoogle Scholar
  8. R, Thirumdas A, Kothakota U, Annapure K, Siliveru R, Blundell R, Gatt VP, Valdramidis (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
  9. Laroussi M, Plasma Medicine (2018) A brief introduction. Plasma 1:47–60. https://doi.org/10.3390/plasma1010005ArticleCASGoogle Scholar
  10. NH, Neuenfeldt LP, Silva RS, Pessoa LO, Rocha (2023) Cold plasma technology for controlling toxigenic fungi and mycotoxins in food. Curr Opin Food Sci 101045. https://doi.org/10.1016/j.cofs.2023.101045
  11. Melo TFd, Rocha LC, Silva RP, Pessoa RS, Negreiros AMP, Sales Júnior R, Tavares MB, Alves Junior C (2022) Plasma–Saline Water Interaction: A Systematic Review Materials 15:4854. https://doi.org/10.3390/ma15144854ArticleCASPubMedGoogle Scholar
  12. Mann MS, Tiede T, Gavenis K, Daeschlein G, Bussiahn R, Weltmann K-D, Emmert S, von Woedtke T, Almed R (2016) Introduction to DIN-specification 91315 based on the characterization of the plasma jet kINPen® MED. Clin Plasma Med 4:35–45 ArticleGoogle Scholar
  13. Gerling T, Helmke A, Weltmann K-D (2018) In: Metelmann H-R et al (eds) Comprehensive clinical plasma medicine: Cold Physical plasma for medical application, 1st edn. Springer International Publishing
  14. A, Lehmann F, Pietag Th, Arnold (2017) Human health risk evaluation of a microwave-driven atmospheric plasma jet as medical device. Clin Plasma Med 7–8. https://doi.org/10.1016/j.cpme.2017.06.001
  15. G (2018) Lessons from Tesla for plasma medicine. IEEE Trans Radiation Plasma Med Sci 2:594–607. https://doi.org/10.1109/TRPMS.2018.2866373
  16. Napp J, Daeschlein G, Napp M, von Podewils S, Gümbel D, Spitzmueller R, Fornaciari P, Hinz P, Jünger M (2015) On the history of plasma treatment and comparison of microbiostatic efficacy of a historical high-frequency plasma device with two modern devices. GMS Hygiene and Infection Control 10. https://doi.org/10.3205/dgkh000251
  17. Daeschlein G, Napp M, von Podewils S, Scholz S, Arnold A, Emmert S, Haase H, Napp J, Spitzmueller R, Gümbel D, Jünger M (2015) Antimicrobial efficacy of a historical high-frequency plasma apparatus in comparison with 2 Modern, Cold Atmospheric pressure plasma Devices. Surg Innov 22:394–400. https://doi.org/10.1177/1553350615573584ArticlePubMedGoogle Scholar
  18. Ishikawa K, Takeda K, Yoshimura S, Kondo T, Tanaka H, Toyokuni S, Nakamura K, Kajiyama H (2023) Masaaki Mizuno and Masaru Hori. “Generation and measurement of low-temperature plasma for cancer therapy: a historical review. Free Radic Res 57:239–270. https://doi.org/10.1080/10715762.2023.2230351ArticleCASPubMedGoogle Scholar
  19. Isbary G, Shimizu T, Li Yang-fang, Stolz W, Thomas HM, Morfill GE, Zimmermann JL (2013) Cold atmospheric plasma devices for medical issues. Expert Rev Med Dev 10:367–377. https://doi.org/10.1586/erd.13.4ArticleCASGoogle Scholar
  20. Reuter S, von Woedtke T, Weltmann K (2018) The kINPen—a review on physics and chemistry of the atmospheric pressure plasma jet and its applications. J Phys D 51. https://doi.org/10.1088/1361-6463/aab3ad
  21. K (2015) Sigrid and Silke Arndt. “Plasma medicine in dermatology: Mechanisms of action and clinical applications” Der Hautarzt; Zeitschrift fur Dermatologie, Venerologie, und verwandte Gebiete 66 11 : 819 – 28. https://doi.org/10.1007/s00105-015-3686-x
  22. Laroussi M (2018) “Plasma Medicine: A Brief Introduction.” 1, 5; https://doi.org/10.3390/plasma1010005
  23. Korzec, Darius Dr, Hoppenthaler F, Nettesheim S (2020) “Piezoelectric Direct Discharge: Devices and Applications.” Plasma : n. pag. https://doi.org/10.3390/plasma4010001
  24. Haertel B, von Woedtke T, Weltmann K, Lindequist U (2014) Non-Thermal Atmospheric-Pressure plasma possible application in Wound Healing, vol 22. Biomolecules & Therapeutics, pp 477–490
  25. Boehm D, Bourke P (2018) Safety implications of plasma-induced effects in living cells – a review of in vitro and in vivo findings. Biol Chem 400:3–17 ArticlePubMedGoogle Scholar
  26. Bernhardt T, Semmler ML, Schäfer M, Bekeschus S, Emmert S, Boeckmann L (2019) Plasma Medicine: Applications of Cold Atmospheric Pressure Plasma in Dermatology. Oxidative Medicine and Cellular Longevity, 2019
  27. Mitra S, Nguyen LN, Akter M, Park G, Choi EH, Kaushik NK (2019) Impact of ROS generated by Chemical, Physical, and plasma techniques on Cancer Attenuation. Cancers, p 11
  28. Dai, Xiaofeng Z, Zhang J, Zhang, Kostya Ken Ostrikov (2020) Dosing: the key to precision plasma oncology. Plasma Processes Polym 17:1900178 ArticleGoogle Scholar
  29. L, Dawei Y, Zhang M, Xu H, Chen X, Lu, Kostya Ken Ostrikov (2020) Cold atmospheric pressure plasmas in dermatology: sources, reactive agents, and therapeutic effects. Plasma Processes Polym 17:1900218
  30. Boeckmann L, Schäfer M, Bernhardt T, Semmler ML, Jung O, Ojak G, Fischer T, Peters K, Nebe B, Müller-Hilke B, Seebauer C, Bekeschus S, Emmert S (2020) Cold Atmospheric pressure plasma in Wound Healing and Cancer Treatment. Applied Sciences
  31. Braný D, Dvorská D, Halasová E, Skovierová H (2020) Cold Atmospheric plasma: a powerful Tool for Modern Medicine. Int J Mol Sci, 21
  32. Semmler ML, Bekeschus S, Schäfer 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):269. https://doi.org/10.3390/cancers12020269ArticleCASPubMedGoogle Scholar
  33. Filipić A, Gutierrez-Aguirre I, Primc G, Mozetič M, Dobnik D (2020) Cold plasma, a New Hope in the field of virus inactivation. Trends Biotechnol 38(11):1278–1291. https://doi.org/10.1016/j.tibtech.2020.04.003ArticleCASPubMedPubMed CentralGoogle Scholar
  34. Busco G, Éric, Robert N, Chettouh-Hammas JM, Pouvesle, Grillon C “The emerging potential of cold atmospheric plasma in skin biology.” Free radical biology & medicine (2020): n. pag. https://doi.org/10.1016/j.freeradbiomed.2020.10.004
  35. Malyavko A, Wang DYanQ, Klein AL, Patel K, Sherman JH, Keidar M (2020) Cold atmospheric plasma cancer treatment, direct versus indirect approaches. Mater Adv. https://doi.org/10.1039/d0ma00329h. n. pag ArticleGoogle Scholar
  36. Domonkos M, Tichá P, Trejbal J, Demo P (2021) Applications of Cold Atmospheric Pressure Plasma Technology in Medicine, Agriculture and Food Industry. Applied Sciences, 11, 4809
  37. Garner AL, Mehlhorn TA (2021) A review of Cold Atmospheric pressure Plasmas for Trauma and Acute Care. Frontiers of Physics
  38. Scholtz V, Vaňková E, Kašparová P, Premanath R, Karunasagar I, Julák J (2021) Non-thermal plasma treatment of ESKAPE Pathogens: a review. Front Microbiol, 12
  39. M-S (2021) Miguel, Juan Tornín, María Pau Ginebra and Cristina Canal. “Cold Atmospheric plasma: a New Strategy based primarily on oxidative stress for Osteosarcoma Therapy. J Clin Med 10. https://doi.org/10.3390/jcm10040893. n. pag
  40. Chen Z, Chen G, Obenchain R, Zhang R, Bai F, Fang T, Wang H, Lu Y, Wirz RE, Gu Z (2022) Cold atmospheric plasma delivery for biomedical applications. Materials Today
  41. Deepak GD, Atul (2022) Biomedical Applications of Cold plasma. Journal Of Clinical And Diagnostic Research
  42. Bhattacharjee B, Bezbaruah R, Rynjah D, Newar A, Sengupta S, Pegu P, Dey N, Bora S, Barman D (2023) Cold Atmospheric plasma: a Noteworthy Approach in Medical Science. Sciences of Pharmacy
  43. Chupradit S, Widjaja G, Radhi Majeed B, Kuznetsova M, Ansari MJ, Suksatan W, Turki Jalil A, Esfahani G, B (2023) Recent advances in cold atmospheric plasma (CAP) for breast cancer therapy. Cell Biol Int 47:327–340. https://doi.org/10.1002/cbin.11939ArticleCASPubMedGoogle Scholar
  44. Chen Z, Bai F, Jonas SJ, Wirz RE (2022) Cold atmospheric plasma for addressing the COVID-19 pandemic. Plasma Process Polym 19:e2200012. https://doi.org/10.1002/ppap.202200012ArticleCASGoogle Scholar
  45. Murillo D, Huergo C, Gallego B, Rodríguez R, Tornín J (2023) Exploring the Use of Cold Atmospheric plasma to Overcome Drug Resistance in Cancer, vol 11. Biomedicines
  46. Singh S, Chandra R, Tripathi SK, Rahman H, Tripathi PK, Jain A, Gupta P (2014) The bright future of dentistry with cold plasma - review. IOSR J Dent Med Sci 13:06–13 ArticleGoogle Scholar
  47. Zhang, Jingqi F, Li K, Lu W, Zhang, Ma J (2023) Recent advances in cold atmospheric plasma for tumor therapy. Process Biochem. https://doi.org/10.1016/j.procbio.2023.06.009. n. pag ArticleGoogle Scholar
  48. Kaushik N, Mitra S, Baek EJ, Nguyen LN, Bhartiya P, Kim June-hyun (2022) Eun ha Choi and Nagendra Kumar Kaushik. “The inactivation and destruction of viruses by reactive oxygen species generated through physical and cold atmospheric plasma techniques: current status and perspectives. J Adv Res 43:59–71. https://doi.org/10.1016/j.jare.2022.03.002ArticleCASPubMedPubMed CentralGoogle Scholar
  49. Dai X, Zhu K (2023) Cold atmospheric plasma: novel opportunities for tumor microenvironment targeting. Cancer Med 12:7189–7206. https://doi.org/10.1002/cam4.5491ArticleCASPubMedPubMed CentralGoogle Scholar
  50. Singh S, Chandra R, Tripathi SK, Rahman H, Tripathi PK, Jain A, Pulkit Gupta (2014) The bright future of dentistry with cold plasma - review. IOSR J Dent Med Sci 13:06–13. https://doi.org/10.9790/0853-131040613ArticleGoogle Scholar
  51. Arora, Nikhil, Nk S, Arora P (2013) Cold Atmospheric plasma (CAP) in Dentistry. Dentistry 3000(4):1–6 Google Scholar
  52. K, Ch S, Sarada PP, Reddy Ch S, Reddy M, S., Dsv N (2014) Plasma torch toothbrush a new insight in fear free dentistry. J Clin Diagn research: JCDR 8(6):ZE07–10
  53. Li H, Zhang X, Zhu X, Zheng M, Liu S, Qi X, Wang K, Chen J, Xi X, Tan J, Ostrikov KK (2017) Translational plasma stomatology: applications of cold atmospheric plasmas in dentistry and their extension
  54. Hui WL, Perrotti V, Iaculli F, Piattelli A, Quaranta A (2020) The emerging role of Cold Atmospheric plasma in Implantology: a review of the literature. Nanomaterials, 10
  55. Awad MM, Alhalabi F, Alshehri A, Aljeaidi ZA, Alrahlah A (2021) Mutlu Özcan and Hamdi Hosni Hamama. “Effect of Non-Thermal Atmospheric plasma on Micro-Tensile Bond Strength at Adhesive/Dentin interface: a systematic review. Materials 14. https://doi.org/10.3390/ma14041026. n. pag
  56. S, Jovana N, Pficer JK, Miličić B (2021) Nevena Puač and Vesna Miletic. “Effects of non-thermal atmospheric plasma on dentin wetting and adhesive bonding efficiency: systematic review and meta-analysis. J Dent 103765. https://doi.org/10.1016/j.jdent.2021.103765
  57. Jungbauer G, Moser D, Müller 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, 10
  58. Borges AC, Kostov KG, Pessoa RS, de Abreu GM, Lima GD, Figueira LW, Koga-Ito CY (2021) Applications of Cold Atmospheric Pressure Plasma in Dentistry. Applied Sciences
  59. Lata S, Chakravorty S, Mitra T, Pradhan PK, Mohanty SK, Patel P, Jha E, Panda PK, Verma SK, Suar M (2021) Aurora borealis in dentistry: the applications of cold plasma in biomedicine. Mater Today Bio, 13
  60. Suresh M, Hemalatha VT, Sundar NM, Nisha AM (2022) Applications of Cold Atmospheric pressure plasma in Dentistry- A Review. Journal of Pharmaceutical Research International
  61. Liu Z, Du X, Xu L, Shi Q, Tang X, Cao Y, Song K (2023 Feb) The therapeutic perspective of cold atmospheric plasma in periodontal disease. Oral Dis 24. https://doi.org/10.1111/odi.14547
  62. Z, Wen Xiu-li, Wang, Huang X (2022) Cold atmospheric pressure plasmas applications in dentistry. Plasma Processes Polym. https://doi.org/10.1002/ppap.202200024. n. pag
  63. M, Bessa A (2023) Mariana Raquel da Cruz Vegian, Lady Daiane Pereira Leite, Diego Morais da Silva, Noala Vicensoto Moreira Milhan, Konstantin Georgiev Kostov and Cristiane Yumi Koga-Ito. “Non-Thermal Atmospheric pressure plasma application in endodontics. Biomedicines 11. https://doi.org/10.3390/biomedicines11051401. n. pag
  64. G, Kamgang-Youbi JM, Herry T, Meylheuc JL, Brisset MN, Bellon-Fontaine A, Doubla M, Naïtali (2009) Microbial inactivation using plasma-activated water obtained by gliding electric discharges. Lett Appl Microbiol 48:13–18. https://doi.org/10.1111/j.1472-765X.2008.02476.x
  65. G, Kamgang-Youbi JM, Herry MN, Bellon-Fontaine JL, Brisset A, Doubla M, Naïtali (2007) Evidence of temporal postdischarge decontamination of bacteria by gliding electric discharges: application to Hafnia alvei. Appl Environ Microbiol 73:4791–4796. https://doi.org/10.1128/AEM.00120-07
  66. AP, Souto FR, Oliveira N, Carneiro (2016) Polyamide 6.6 modified by DBD plasma treatment for anionic dyeing processes. Intech 13. https://doi.org/10.5772/57353
  67. P, Cools S, Van Vrekhem N, De Geyter R, Morent (2014) The use of DBD plasma treatment and polymerization for the enhancement of biomedical UHMWPE. Thin Solid Films 572:251–259. https://doi.org/10.1016/j.tsf.2014.08.033
  68. F, Judée S, Simon C, Bailly T, Dufour (2018) Plasma-activation of tap water using DBD for agronomy applications: identification and quantification of long lifetime chemical species and production/consumption mechanisms. Water Res 133:47–59. https://doi.org/10.1016/j.watres.2017.12.035
  69. T, Royintarat P, Seesuriyachan D, Boonyawan EH, Choi W, Wattanutchariya (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 19:1006–1014. https://doi.org/10.1016/j.cap.2019.05.020
  70. V, Straňák P, Spatenka MT, Tich´y J, Koller V, Kříha V, Scholtz Surfatron plasma-based sterilisation, n.d
  71. M, Dharini S, Jaspin R, Mahendran (2023) Cold plasma reactive species: Generation, properties, and interaction with food biomolecules. Food Chem 405. https://doi.org/10.1016/j.foodchem.2022.134746
  72. C, Hoffmann C, Berganza J, Zhang, Cold Atmospheric Plasma (2013) Methods of production and application in dentistry and oncology. Med Gas Res 3:1–15. https://doi.org/10.1186/2045-9912-3-21
  73. A, Schmidt S, Bekeschus K, Wende B, Vollmar T, von Woedtke (2017) A cold plasma jet accelerates wound healing in a murine model of full-thickness skin wounds. Exp Dermatol 26:156–162. https://doi.org/10.1111/exd.13156
  74. BE, Konelschatz WEAU, Principle, Applications (1997) J PHYS IV FRANCE 7:7
  75. W, Zhou P, Xiao Y, Li L, Zhou (2013) Dielectric properties of BN modified carbon fibers by dip-coating. Ceram Int 39:6569–6576. https://doi.org/10.1016/j.ceramint.2013.01.090
  76. H-J, Lee S, Jung H-S, Jung S-H, Park W-H, Choe J-S, Ham C, Jo (2012) Evaluation of a dielectric barrier discharge plasma system for inactivating pathogens on cheese slices. J Anim Sci Technol 54:191–198. https://doi.org/10.5187/jast.2012.54.3.191
  77. S, Mohades AM, Lietz MJ, Kushner (2020) Generation of reactive species in water film dielectric barrier discharges sustained in argon, helium, air, oxygen and nitrogen. J Phys D Appl Phys 53. https://doi.org/10.1088/1361-6463/aba21a
  78. A, Fridman S, Nester LA, Kennedy A, Saveliev O, Mutaf-Yardimci PII: S0360-1285(98)00021-5, (n.d.)
  79. A (2008) Fridman, Plasma chemistry, Cambridge university press,
  80. R, Burlica MJ, Kirkpatrick BR, Locke (2006) Formation of reactive species in gliding arc discharges with liquid water. J Electrostat 64:35–43. https://doi.org/10.1016/j.elstat.2004.12.007
  81. J, Pawłat P, Terebun M, Kwiatkowski B, Tarabová Z, Kovaľová K, Kučerová Z, Machala M, Janda K, Hensel (2019) Evaluation of oxidative species in Gaseous and Liquid Phase generated by Mini-Gliding Arc Discharge, plasma Chemistry and plasma Processing. https://doi.org/10.1007/s11090-019-09974-9
  82. B, Riviere J-M, Mermet D, Deruaz (1989) Behaviour and Analytical Applications of a Modulated Power Microwave-induced Plasma (Surfatron),
  83. K, Kutasi D, Popović N, Krstulović S, Milošević (2019) Tuning the composition of plasma-activated water by a surface-wave microwave discharge and a kHz plasma jet. Plasma Sources Sci Technol 28. https://doi.org/10.1088/1361-6595/ab3c2f
  84. U, Kogelschatz B, Eliasson W, Egli U, Kogelschatz B, Eliasson WEDD, Principle (1997) Dielectric-Barrier Discharges. Principle and Applications To cite this version: HAL Id: jpa-00255561,
  85. F, Gasi G, Petraconi E, Bittencourt SR, Lourenço AHR, Castro F, de Miranda S, Essiptchouk AM, Nascimento L, Petraconi A, Fraga MA, Pessoa RS (2020) Plasma treatment of Polyamide Fabric Surface by Hybrid Corona-Dielectric Barrier Discharge: material characterization and Dyeing/Washing processes. Mater Res 23:1–9. https://doi.org/10.1590/1980-5373-mr-2019-0255
  86. S, Portugal B, Choudhury D, Cardenas (2022) Advances on aerodynamic actuation induced by surface dielectric barrier discharges. Front Phys 10. https://doi.org/10.3389/fphy.2022.923103
  87. PIV, France E, Abb (1997) Dielectric-barrier discharges. Principle and Applications, 7
  88. S, Wu Y, Cao X, Lu (2016) The state of the art of Applications of Atmospheric-Pressure nonequilibrium plasma jets in Dentistry. IEEE Trans Plasma Sci 44:134–151. https://doi.org/10.1109/TPS.2015.2506658
  89. R, Laurita D, Barbieri M, Gherardi V, Colombo P, Lukes (2015) Chemical analysis of reactive species and antimicrobial activity of water treated by nanosecond pulsed DBD air plasma. Clin Plasma Med 3:53–61. https://doi.org/10.1016/j.cpme.2015.10.001
  90. UK, Ercan B, Sen AD, Brooks SG, Joshi (2018) Escherichia coli cellular responses to exposure to atmospheric-pressure dielectric barrier discharge plasma-treated N-acetylcysteine solution. J Appl Microbiol 125:383–397. https://doi.org/10.1111/jam.13777
  91. V, Luvita AT, Sugiarto S, Bismo (2022) Characterization of dielectric barrier discharge reactor with nanobubble application for industrial water treatment and depollution. S Afr J Chem Eng 40:246–257. https://doi.org/10.1016/j.sajce.2022.03.009
  92. M, Vadivel S, Shobana SA, Narayan L, Mitu JD, Raja M, Sankarganesh (2017) Optimization of process conditions and characterization of ethylene-propylene-diene rubber with bismaleimide. Bul Chem Commun 49:26–30
  93. A, Pedro F, Ribeiro N, Carneiro (2011) Polyamide 6.6 modified by DBD plasma treatment for anionic dyeing processes, Textile Dyeing. https://doi.org/10.5772/21755
  94. YD, Korolev (2015) Low-current discharge plasma jets in a gas flow. Application of plasma jets. Russ J Gen Chem 85:1311–1325. https://doi.org/10.1134/S1070363215050473
  95. G, Kamgang-Youbi JM, Herry T, Meylheuc JL, Brisset MN, Bellon-Fontaine A, Doubla M, Naïtali (2009) Microbial inactivation using plasma-activated water obtained by gliding electric discharges. Lett Appl Microbiol 48:13–18. https://doi.org/10.1111/j.1472-765X.2008.02476.x
  96. G, Kamgang-Youbi JM, Herry MN, Bellon-Fontaine JL, Brisset A, Doubla M, Naïtali (2007) Evidence of temporal postdischarge decontamination of bacteria by gliding electric discharges: application to Hafnia alvei. Appl Environ Microbiol 73:4791–4796. https://doi.org/10.1128/AEM.00120-07
  97. ACOC, Doria CPC, Sorge TB, Santos J, Brandão PAR, Gonçalves HS, Maciel S, Khouri RS, Pessoa (2015) Application of post-discharge region of atmospheric pressure argon and air plasma jet in the contamination control of Candida albicans biofilms. Res Biomed Eng 31(4). https://doi.org/10.1590/2446-4740.01215
  98. ACOC, Doria FR, Figueira JSB, de Lima JAN, Figueira AHR, Castro BN, Sismanoglu G, Petraconi HS, Maciel S, Khouri RS, Pessoa Inactivation of Candida albicans biofilms by atmospheric gliding arc plasma jet: effect of gas chemistry/flow and plasma pulsing, Plasma Res Express 1 015001. https://doi.org/10.1088/2516-1067/aae7e1
  99. GG, Bălan I, Roşca EL, Ursu F, Doroftei AC, Bostănaru E, Hnatiuc V, Năstasă V, Şandru G, Ştefănescu A, Trifan M, Mareş (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
  100. MJ, Traylor MJ, Pavlovich S, Karim P, Hait Y, Sakiyama DS, Clark DB, Graves (2011) Long-term antibacterial efficacy of air plasma-activated water. J Phys D Appl Phys 44. https://doi.org/10.1088/0022-3727/44/47/472001
  101. YM, Zhao S, Ojha CM, Burgess DW, Sun BK, Tiwari (2021) Inactivation efficacy of plasma-activated water: influence of plasma treatment time, exposure time and bacterial species. Int J Food Sci Technol 56:721–732. https://doi.org/10.1111/ijfs.14708
  102. X, Lu GV, Naidis M, Laroussi S, Reuter DB, Graves K, Ostrikov (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
  103. YM, Zhao A, Patange DW, Sun B, Tiwari (2020) Plasma-activated water: physicochemical properties, microbial inactivation mechanisms, factors influencing antimicrobial effectiveness, and applications in the food industry. Compr Rev Food Sci Food Saf 19:3951–3979. https://doi.org/10.1111/1541-4337.12644
  104. R, Ma G, Wang Y, Tian K, Wang J, Zhang J, Fang (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
  105. Q, Xiang L, Fan Y, Li S, Dong K, Li Y, Bai (2020) A review on recent advances in plasma-activated water for food safety: current applications and future trends. Crit Rev Food Sci Nutr. https://doi.org/10.1080/10408398.2020.1852173
  106. A, Soni J, Choi G, Brightwell (2021) Plasma-activated water (PAW) as a disinfection technology for bacterial inactivation with a focus on fruit and vegetables, Foods. 10 https://doi.org/10.3390/foods10010166
  107. J, Wang R, Han X, Liao T, Ding (2021) Application of plasma-activated water (PAW) for mitigating methicillin-resistant Staphylococcus aureus (MRSA) on cooked chicken surface. Lwt 137:110465. https://doi.org/10.1016/j.lwt.2020.110465
  108. Y, Li J, Pan G, Ye Q, Zhang J, Wang J, Zhang J, Fang (2017) In vitro studies of the antimicrobial effect of non-thermal plasma-activated water as a novel mouthwash, Eur J Oral Sci. 125 463–470. https://doi.org/10.1111/eos.12374
  109. , DIN SPEC 91315 (2014), General Requirements For Plasma Sources In Medicine, pp. 1–16
  110. L, Eisner RM, Brown D, Modi (2004) Leakage Current Standards Simplified. MDDI in Regulatory and Compliance,
  111. KG, Kostov et al (2010) “Bacterial sterilization by a dielectric barrier discharge (DBD) in air,” Surface and Coatings Technology, vol. 204, no. 18, pp. 2954–2959, doi: https://doi.org/10.1016/j.surfcoat.2010.01.052
  112. TMC, Nishime “Development and characterization of extended and flexible plasma jets,” PhD thesis, São Paulo State University–UNESP, Guaratinguetá, São Paulo, Brazil, 2019. [Online]. Available: https://repositorio.unesp.br/bitstream/handle/11449/190654/nishime_tmc_dr_guara_int.pdf?sequence=4&isAllowed=y
  113. KG, Kostov M, Machida V, Prysiazhnyi, Honda RY (Apr. 2015) Transfer of a cold atmospheric pressure plasma jet through a long flexible plastic tube. Plasma Sources Sci Technol 24(2):025038. https://doi.org/10.1088/0963-0252/24/2/025038
  114. Y, Xia et al (Jan. 2016) The transfer of atmospheric-pressure ionization waves via a metal wire. Phys Plasmas 23(1):013509. https://doi.org/10.1063/1.4940332
  115. O, Bastin et al (2020) Optical and electrical characteristics of an endoscopic DBD plasma jet. PMED 10(2):71–90. https://doi.org/10.1615/PlasmaMed.2020034526
  116. KG, Kostov TMC, Nishime M, Machida AC, Borges V, Prysiazhnyi, Koga-Ito CY (2015) Study of Cold Atmospheric plasma jet at the end of Flexible Plastic Tube for Microbial Decontamination. Plasma Processes Polym 12(12):1383–1391. https://doi.org/10.1002/ppap.201500125
  117. TMC, Nishime AC, Borges CY, Koga-Ito M, Machida LRO, Hein, Kostov KG (2017) “Non-thermal atmospheric pressure plasma jet applied to inactivation of different microorganisms,” Surface and Coatings Technology, vol. 312, pp. 19–24, Feb. doi: https://doi.org/10.1016/j.surfcoat.2016.07.076
  118. AC, Borges et al (2017) “Cold atmospheric pressure plasma jet modulates Candida albicans virulence traits,” Clinical Plasma Medicine, vol. 7–8, pp. 9–15, doi: https://doi.org/10.1016/j.cpme.2017.06.002
  119. AC, Borges G, de Lima MG, 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, vol. 13, no. 6, p. e0199832, Jun. doi: https://doi.org/10.1371/journal.pone.0199832
  120. AC, Borges et al (2019) “Cold Atmospheric Pressure Plasma Jet Reduces Trichophyton rubrum Adherence and Infection Capacity,” Mycopathologia, vol. 184, no. 5, pp. 585–595, doi: https://doi.org/10.1007/s11046-019-00375-2
  121. LDP, Leite et al (2021) “Effect of Cold Atmospheric Plasma Jet Associated to Polyene Antifungals on Candida albicans Biofilms,” Molecules, vol. 26, no. 19, Art. no. 19, doi: https://doi.org/10.3390/molecules26195815
  122. G, de Lima MG et al (2021) Cold Atmospheric plasma jet as a possible adjuvant therapy for Periodontal Disease. Molecules 26 18, Art. no. 18, Jan. https://doi.org/10.3390/molecules26185590
  123. MAC, de Oliveira et al (2021) “Inhibitory Effect of Cold Atmospheric Plasma on Chronic Wound-Related Multispecies Biofilms,” Applied Sciences, vol. 11, no. 12, Art. no. 12, doi: https://doi.org/10.3390/app11125441
  124. G (2022) de Morais Gouvêa Lima, “Cold Atmospheric Pressure Plasma Is Effective against P. gingivalis (HW24D-1) Mature Biofilms and Non-Genotoxic to Oral Cells,” Applied Sciences, vol. 12, no. 14, Art. no. 14, doi: https://doi.org/10.3390/app12147247
  125. F, do Nascimento KG, Kostov M, Machida, Flacker A (2021) “Properties of DBD Plasma Jets Using Powered Electrode With and Without Contact With the Plasma,” IEEE Transactions on Plasma Science, vol. 49, no. 4, pp. 1293–1301, Apr. doi: https://doi.org/10.1109/TPS.2021.3067159
  126. F, do Nascimento T, Gerling, Kostov KG (Apr. 2023) On the gas heating effect of helium atmospheric pressure plasma jet. Phys Scr 98(5):055013. https://doi.org/10.1088/1402-4896/accb17
  127. F, do Nascimento BS, Leal A, Quade, Kostov KG (Jan. 2022) Different radial modification profiles observed on APPJ-Treated polypropylene surfaces according to the Distance between plasma outlet and target. Polymers 14 no. 21, Art. no. 21. https://doi.org/10.3390/polym14214524
  128. F, do Nascimento A, Quade MA, Canesqui, Kostov KG (2023) “Different configurations of transferred atmospheric pressure plasma jet and their application to polymer treatment,” Contributions to Plasma Physics, vol. 63, no. 1, p. e202200055, doi: https://doi.org/10.1002/ctpp.202200055
  129. Rao Y, Shang W, Yang Y, Zhou R, Rao X (2020) Fighting mixed-species microbial Biofilms with Cold Atmospheric plasma. Front Microbiol 11:11. https://doi.org/10.3389/fmicb.2020.01000ArticleGoogle Scholar
  130. KG, Kostov V, Rocha CY, Koga-Ito MA, Algatti RY, Honda ME, Kayama RP, Mota (2010) Surf Coat Technol 204:18
  131. TMC, Nishime AC, Borges CY, Koga-Ito M, Munemasa LRO, Hein KG, Kostov (2017) Surf Coat Technol 1:19
  132. AC, Borges TMC, Nishime SM, Rovetta GMG, Lima KG, Kostov GP, Thim BR, Menezes JPB, Machado CY (2019) Koga-Ito Mycopathologia 184:585
  133. Z, Wang M, Zhu D, Liu L, Liu X, Wang J, Chen L, Guo Y, Liu M, Hou M, Rong (2023) N2O5 in air discharge plasma: energy-efficient production, maintenance factors and sterilization effects. J Phys D Appl Phys 56. https://doi.org/10.1088/1361-6463/acb65f
  134. M, Moreau N, Orange MGJ, Feuilloley (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
  135. Sakudo A, Yagyu Y, Onodera T (2019) Disinfection and sterilization using plasma technology: Fundamentals and Future Perspectives for Biological Applications. Int J Mol Sci 20(20):5216. https://doi.org/10.3390/ijms20205216ArticleCASPubMedPubMed CentralGoogle Scholar
  136. Chen Z, Garcia G Jr, Arumugaswami V, Wirz RE (2020) Cold atmospheric plasma for SARS-CoV-2 inactivation. Phys Fluids (1994) 32(11):111702. https://doi.org/10.1063/5.0031332ArticleCASPubMedGoogle Scholar
  137. Volotskova O, Dubrovsky L, Keidar M, Bukrinsky M (2016) Cold Atmospheric plasma inhibits HIV-1 replication in Macrophages by Targeting both the Virus and the cells. PLoS ONE 11(10):e0165322. https://doi.org/10.1371/journal.pone.0165322ArticleCASPubMedPubMed CentralGoogle Scholar
  138. Ciofu O, Moser C, Jensen P, Høiby N (2022) Tolerance and resistance of microbial biofilms. In Nature Reviews Microbiology (Vol. 20, Issue 10, pp. 621–635). Nature Research. https://doi.org/10.1038/s41579-022-00682-4
  139. Eming SA, Martin P, Tomic-Canic M (2014) Wound repair and regeneration: mechanisms, signaling and translation. Sci Transl Med 6(265):265sr6. https://doi.org/10.1126/scitranslmed.3009337ArticleCASPubMedPubMed CentralGoogle Scholar
  140. MAC, Oliveira GMG, Lima TMC, Nishime AVL, Gontijo MBRC, Menezes MV, Caliari KG, Kostov CY (2021) Koga-Ito, Applied Sciences, 11, 5441
  141. Lee MH, Lee YS, Kim HJ, Han CH, Kang SU, Kim CH (2019) Non-thermal plasma inhibits mast cell activation and ameliorates allergic skin inflammatory diseases in NC/Nga mice. Sci Rep 9:1–10. https://doi.org/10.1038/s41598-019-49938-9ArticleCASGoogle Scholar
  142. Xiong Q, Wang X, Yin R, Xiong L, Chen Q, Zheng MX, Xu L, Huang QH, Hamblin MR (2018) Surface treatment with non-thermal humid argon plasma as a treatment for allergic contact Dermatitis in a mouse model. Clin Plasma Med 12:10–16. https://doi.org/10.1016/j.cpme.2018.09.002ArticlePubMedPubMed CentralGoogle Scholar
  143. VN, Vasilets (2019) Plasmachemical generation of nitric oxides in air plasmas for medical applications. ChemChemTech 62:4–13. https://doi.org/10.6060/ivkkt.20196205.5958
  144. MD, Nguyen QT, Do TT, Luong NT, Le TT, Nguyen TP, Bui HT, Do H, Metelmann C, Seebauer TT, Vu (2020) Cold atmospheric plasma treatment on failed finger perforator flap: a case report. Clin Plasma Med 19–20. https://doi.org/10.1016/j.cpme.2020.100105
  145. Benova E, Topalova Y, Marinova P, Todorova Y, Atanasova M, Bogdanov T, Yotinov I Surface-wave-sustained plasma for model biological systems treatment. In Proceedings of the XXXIII International Conference on Phenomena in Ionized Gases (ICPIG), Estoril, Portugal, 9–14 July 2017; Alves, L.L., Tejero-del-Caz, A., Eds.; Instituto de Plasmas e Fusão Nuclear, Instituto Superior Técnico, Universidade de Lisboa: Lisboa, Portugal, 2017. Topic Number: 17. p. 87
  146. Tsvetkov V, Hinkov A, Todorov D, Benova E, Tsonev I, Bogdanov T, Shishkov S, Shishkova K (2019) Effect of plasma-activated medium and water on replication and extracellular virions of herpes simplex Virus-1. Plasma Med 9:205–216 Google Scholar
  147. Arndt S, Schmidt A, Karrer S, VonWoedtke T (2018) Comparing two different plasma devices kINPen and Adtec SteriPlas regarding their molecular and cellular effects on wound healing. Clin Plasma Med 9:24–33 ArticleGoogle Scholar
  148. Bogdanov T, Tsonev I, Traikov LL (2020) Microwave plasma torch for wound treatment. J Phys Conf Ser 1598:012001 ArticleGoogle Scholar
  149. Krcma F, Tsonev I, Smejkalová K, Truchlá D, Kozáková Z, Zhekova M, Marinova P, Bogdanov T, Benova E (2018) Microwave micro torch generated in argon based mixtures for biomedical applications. J Phys D Appl Phys 51:414001 ArticleGoogle Scholar
  150. Pitts NB, Zero DT, Marsh PD, Ekstrand K, Weintraub JA, Ramos-Gomez F, Tagami J, Twetman S, Tsakos G, Ismail A (2017) Dental caries. Nat Reviews Disease Primers 3. https://doi.org/10.1038/nrdp.2017.30
  151. Jungbauer G, Moser D, Müller 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. Antibiot (Basel) 10(2):211. https://doi.org/10.3390/antibiotics10020211ArticleCASGoogle Scholar
  152. GMG, Lima CFL, Carta AC, Borges TMC, Nishime CAV, Silva MV, Caliari MP, Mayer KG, Kostov (2022) C.Y. Koga-Ito, Applied Sciences, 12, 7247
  153. 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.12083ArticleCASPubMedPubMed CentralGoogle Scholar
  154. KG, Kostov AC, Borges CY, Koga-Ito TMC, Nishime V, Prysiazhnyi RI, Honda (2015) IEEE Trans Plasma Sci 43:770
  155. AC, Borges TMC, Nishime KG, Kostov GMG, Lima AVL, Gontijo JNMM, Carvalho RI, Honda CY (2017) Koga-Ito. Clin Plasma Med 7:9
  156. AC, Borges GMG, Lima TMC, Nishime AVL, Gontijo KG, Kostov CY (2018) Koga-Ito Plos One 13:0199832
  157. Ebrahimi-Shaghaghi F, Noormohammadi Z, Atyabi SM, Razzaghi-Abyaneh M (2021) Inhibitory effects of cold atmospheric plasma on the growth, virulence factors and HSP90 gene expression in Candida albicans. Arch Biochem Biophys 700:108772 ArticleCASPubMedGoogle Scholar
  158. Kinane DF, Stathopoulou PG, Papapanou PN (2017) Periodontal diseases. Nat Rev Dis Primers 3:17038. https://doi.org/10.1038/nrdp.2017.38ArticlePubMedGoogle Scholar
  159. GMG, Lima AC, Borges TMC, Nishime GF, Santana-Melo KG, Kostov MP, Mayer CY (2021) Koga-Ito Molecules 26:5590
  160. Liu Z, Du X, Xu L, Shi Q, Tang X, Cao Y, Song K (2023 Feb) The therapeutic perspective of cold atmospheric plasma in periodontal disease. Oral Dis 24. https://doi.org/10.1111/odi.14547
  161. Seebauer C, Freund E, Hasse S, Miller V, Segebarth M, Lucas C, Kindler S, Dieke T, Metelmann HR, Daeschlein G, Jesse K, Weltmann KD, Bekeschus S (2021) Effects of cold physical plasma on oral lichen planus: an in vitro study (Effects of CAP on OLP). Oral Dis 27(7):1728–1737. https://doi.org/10.1111/odi.13697ArticlePubMedGoogle Scholar
  162. Semmler ML, Bekeschus S, Schäfer 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):269. https://doi.org/10.3390/cancers12020269ArticleCASPubMedGoogle Scholar
  163. Murillo D, Huergo C, Gallego B, Rodríguez R, Tornín J (2023) Exploring the Use of Cold Atmospheric plasma to Overcome Drug Resistance in Cancer. Biomedicines 11(1):208. https://doi.org/10.3390/biomedicines11010208ArticleCASPubMedPubMed CentralGoogle Scholar
  164. Bugshan A, Farooq I (2020) Oral squamous cell carcinoma: metastasis, potentially associated malignant disorders, etiology and recent advancements in diagnosis. F1000Res 9:229. https://doi.org/10.12688/f1000researchArticleCASPubMedPubMed CentralGoogle Scholar
  165. Metelmann HR, Seebauer C, Miller V, Fridman A, Bauer G, Graves DB et al (2018) Clinical experience with cold plasma in the treatment of locally advanced head and neck cancer. Clin Plasma Med 9:6–13. https://doi.org/10.1016/j.cpme.2017.09.001ArticleGoogle Scholar
  166. Li X, Rui X, Li D, Wang Y, Tan F (2022) Plasma oncology: adjuvant therapy for head and neck cancer using cold atmospheric plasma. Front Oncol 12:994172. https://doi.org/10.3389/fonc.2022.994172ArticleCASPubMedPubMed CentralGoogle Scholar
  167. Wagner G, Eggers B, Duddeck D, Kramer FJ, Bourauel C, Jepsen S, Deschner J, Nokhbehsaim M (2022) Influence of cold atmospheric plasma on dental implant materials - an in vitro analysis. Clin Oral Investig 26(3):2949–2963. https://doi.org/10.1007/s00784-021-04277-wArticlePubMedGoogle Scholar
  168. Kochar SP, Reche A, Paul P (2022) The etiology and management of Dental Implant failure: a review. Cureus 14(10):e30455. https://doi.org/10.7759/cureus.30455PMID: 36415394; PMCID: PMC9674049 ArticlePubMedPubMed CentralGoogle Scholar
  169. Nam SH, Lee HW, Cho SH, Lee JK, Jeon YC, Kim GC (2013) High-efficiency tooth bleaching using non-thermal atmospheric pressure plasma with low concentration of hydrogen peroxide. J Appl Oral Sci 21(3):265–270. https://doi.org/10.1590/1679-775720130016PMID: 23857658; PMCID: PMC3881910 ArticleCASPubMedPubMed CentralGoogle Scholar
  170. KG, Kostov TMC, Nishime M, Machida AC, Borges V, Prysiazhnyi CY (2015) Koga-Ito Plasma Processes and Polymers 12:1383
  171. Chiappim W, Sampaio A, da Miranda G, Fraga F, Petraconi M, da Silva Sobrinho G, Kostov A, Koga-Ito K, Pessoa C (2021) Antimicrobial effect of plasma‐activated tap water on staphylococcus aureus, escherichia coli, and Candida albicans. Water (Switzerland) 13:1480. https://doi.org/10.3390/w13111480ArticleCASGoogle Scholar
  172. W, Chiappim AG, Sampaio F, Miranda M, Fraga G, Petraconi A, Silva Sobrinho P, Cardoso KG, Kostov CY, Koga-Ito (2021) R Pessoa Plasma Processes and Polymers 210001:14
  173. AG, Sampaio W, Chiappim NV, Moreira B, Botan Neto R, Pessoa CY (2022) Koga-Ito. Int J Mol Sci 23:13893
  174. Mai-Prochnow A, Zhou R, Zhang T et al (2021) Interactions of plasma-activated water with biofilms: inactivation, dispersal effects and mechanisms of action. npj Biofilms Microbiomes 7:11. https://doi.org/10.1038/s41522-020-00180-6ArticleCASPubMedPubMed CentralGoogle Scholar
  175. Naïtali M, Kamgang-Youbi G, Herry J‐M, Bellon‐Fontaine M‐N, Brisset J‐L (2010) Combined effects of long‐living chemical species during microbial inactivation using atmospheric plasma‐treated water. Appl Environ Microbiol 76:7662–7664. https://doi.org/10.1128/AEM.01615-10ArticleCASPubMedPubMed CentralGoogle Scholar
  176. 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/srep28505ArticleCASPubMedPubMed CentralGoogle Scholar
  177. 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 37:1091–1103. https://doi.org/10.1007/s11090-017-9811-0ArticleCASGoogle Scholar
  178. Bălan GG, Roşca I, Ursu EL, Doroftei F, Bostănaru AC, Hnatiuc E, Năstasă V, Şandru V, Ştefănescu G, Trifan A et al (2018) Plasma-activated water: a new and effective alternative for duodenoscope reprocessing. Infect Drug Resist 11:727–733. https://doi.org/10.2147/IDR.S159243ArticlePubMedPubMed CentralGoogle Scholar
  179. Gabrilska RA, Rumbaugh KP (2015) Biofilm models of polymicrobial infection. Future Microbiol 10:1997–2015. https://doi.org/10.2217/fmb.15.109ArticleCASPubMedPubMed CentralGoogle Scholar
  180. 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 125:463–470. https://doi.org/10.1111/eos.12374ArticleCASPubMedGoogle Scholar
  181. Hong Q, Dong X, Yu H, Sun H, Chen M, Wang Y, Yu Q (2021) The Antimicrobial Property of plasma activated liquids (PALs) against oral Bacteria streptococcus mutans. Dental 3:1–7. https://doi.org/10.35702/dent.10007ArticleGoogle Scholar
  182. 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 3:53–61. https://doi.org/10.1016/j.cpme.2015.10.001ArticleGoogle Scholar
  183. 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 39:35–49. https://doi.org/10.1007/s11090-018-9930-2ArticleCASGoogle Scholar
  184. G-J, Júnior E, Fardin AC, Gaetti‐Jardim EC, de Castro AL, Schweitzer CM, Avila‐Campos MJ (2010) Microbiota associated with chronic osteomyelitis of the jaws. Brazilian J Microbiol 41:1056–1064. https://doi.org/10.1590/S1517-83822010000400025
  185. Dobrynin D, Fridman G, Friedman G, Fridman A (2009) Physical and biological mechanisms of direct plasma interaction with living tissue. New J Phys 11. https://doi.org/10.1088/1367-2630/11/11/115020
  186. Nastasa V, Pasca A-S, Malancus R‐N, Bostanaru A‐C, Ailincai L‐I, Ursu E‐L, Vasiliu A‐L, Minea B, Hnatiuc E, Mares M (2021) Toxicity Assessment of Long‐Term exposure to non‐thermal plasma activated Water in mice. Int J Mol Sci 22:11534. https://doi.org/10.3390/ijms222111534ArticleCASPubMedPubMed CentralGoogle Scholar
  187. Lee MH, Lee YS, Kim HJ, Han CH, Kang SU, Kim CH (2019) Non-thermal plasma inhibits mast cell activation and ameliorates allergic skin inflammatory diseases in NC/Nga mice. Sci Rep 9:1–10. https://doi.org/10.1038/s41598-019-49938-9ArticleCASGoogle Scholar
  188. Lou BS, Hsieh JH, Chen CM, Hou CW, Wu HY, Chou PY, Lai CH, Lee JW (2020) Helium/Argon-Generated Cold Atmospheric plasma facilitates cutaneous Wound Healing. Front Bioeng Biotechnol 8:1–11. https://doi.org/10.3389/fbioe.2020.00683ArticleGoogle Scholar
  189. Zhang Y, Xiong Y, Xie P, Ao X, Zheng Z, Dong X, Li H, Yu Q, Zhu Z, Chen M et al (2018) Non-thermal plasma reduces periodontitis-induced alveolar bone loss in rats. Biochem Biophys Res Commun 503:2040–2046. https://doi.org/10.1016/j.bbrc.2018.07.154ArticleCASPubMedGoogle Scholar
  190. Eggers B, Marciniak J, Memmert S, Kramer FJ, Deschner J, Nokhbehsaim M (2020) The beneficial effect of cold atmospheric plasma on parameters of molecules and cell function involved in wound healing in human osteoblast-like cells in vitro. Odontology 108:607–616. https://doi.org/10.1007/s10266-020-00487-yArticleCASPubMedPubMed CentralGoogle Scholar
  191. Rezaei F, Vanraes P, Nikiforov A, Morent R, Geyter N (2019) De Appl Plasma-Liquid Systems: Rev Mater 12:2751 CASGoogle Scholar
  192. Nakamura K, Peng Y, Utsumi F, Tanaka H, Mizuno M, Toyokuni S, Hori M, Kikkawa F, Kajiyama H (2017) Novel intraperitoneal treatment with non-thermal plasma-activated medium inhibits metastatic potential of ovarian Cancer cells. Sci Rep 7:1–14. https://doi.org/10.1038/s41598-017-05620-6ArticleCASGoogle Scholar
  193. Tanaka H, Bekeschus S, Yan D, Hori M, Keidar M, Laroussi M, Rns ROS, Rns ROS, Rns ROS (2021) Plasma-treated solutions (PTS) in Cancer Therapy. Cancers 13:1737 ArticleCASPubMedPubMed CentralGoogle Scholar
  194. Shi L, Yu L, Zou F, Hu H, Liu K, Lin Z (2017) Gene expression profiling and functional analysis reveals that p53 pathway-related gene expression is highly activated in cancer cells treated by cold atmospheric plasma‐activated medium. PeerJ 5:e3751. https://doi.org/10.7717/peerj.3751ArticleCASPubMedPubMed CentralGoogle Scholar

Funding

The authors acknowledge financial support from The São Paulo State Research Foundation (FAPESP, grants 2016/07196-6 and 2019/05856-7; fellowships 21/14181-3, 21/00046 − 7, 20/09481-5, and 23/02268-2) and Brazilian National Council for Scientific and Technological Development (309762/2021-9).

Author information

Authors and Affiliations

  1. Department of Environment Engineering, Institute of Science and Technology, São Paulo State University (UNESP), São José dos Campos, Brazil Cristiane Yumi Koga-Ito, F. S. Miranda & N. V.M. Milhan
  2. Department of Physics, Guaratinguetá Faculty of Engineering, São Paulo State University (UNESP), Guaratinguetá, Brazil K. G. Kostov & F. Nascimento
  3. Plasmas and Processes Laboratory (LPP), Aeronautics Institute of Technology (ITA), São José dos Campos, Brazil N. F. Azevedo Neto & R. S. Pessoa
  1. Cristiane Yumi Koga-Ito