Cold Atmospheric Plasma: A Powerful Tool for Modern Medicine

Dušan Braný, Dana Dvorská, Erika Halašová, Henrieta Škovierová, Dušan Braný, Dana Dvorská, Erika Halašová, Henrieta Škovierová

Abstract

Cold atmospheric plasma use in clinical studies is mainly limited to the treatment of chronic wounds, but its application in a wide range of medical fields is now the goal of many analyses. It is therefore likely that its application spectrum will be expanded in the future. Cold atmospheric plasma has been shown to reduce microbial load without any known significant negative effects on healthy tissues, and this should enhance its possible application to any microbial infection site. It has also been shown to have anti-tumour effects. In addition, it acts proliferatively on stem cells and other cultivated cells, and the highly increased nitric oxide levels have a very important effect on this proliferation. Cold atmospheric plasma use may also have a beneficial effect on immunotherapy in cancer patients. Finally, it is possible that the use of plasma devices will not remain limited to surface structures, because current endeavours to develop sufficiently miniature microplasma devices could very likely lead to its application in subcutaneous and internal structures. This study summarises the available literature on cold plasma action mechanisms and analyses of its current in vivo and in vitro use, primarily in the fields of regenerative and dental medicine and oncology.

Keywords: cold atmospheric plasma; oncology; plasma; regenerative medicine; wound healing.

Conflict of interest statement

Authors declare that they have no conflict of interest.

References

    1. Langmuir I. Oscillations in Ionized Gases. Proc. Natl. Acad. Sci. USA. 1928;14:627–637. doi: 10.1073/pnas.14.8.627.
    1. Lee H.W., Park G.Y., Seo Y.S., Im Y.H., Shim S.B., Lee H.J. Modelling of Atmospheric Pressure Plasmas for Biomedical Applications. J. Phys. D. 2011;44:053001. doi: 10.1088/0022-3727/44/5/053001.
    1. Izadjoo M., Zack S., Kim H., Skiba J. Medical Applications of Cold Atmospheric Plasma: State of the Science. J. Wound Care. 2018;27:S4–S10. doi: 10.12968/jowc.2018.27.Sup9.S4.
    1. Bernhardt T., Semmler M.L., Schäfer M., Bekeschus S., Emmert S., Boeckmann L. Plasma Medicine: Applications of Cold Atmospheric Pressure Plasma in Dermatology. Oxidative Med. Cell. Longev. 2019;201:1–10. doi: 10.1155/2019/3873928.
    1. Adhikari B.R., Khanal R. Introduction to the Plasma State of Matter. Himal. Phys. 2013;4:60–64. doi: 10.3126/hj.v4i0.9430.
    1. Bittencourt J.A. Fundamentals of Plasma Physics. Springer; New York, NY, USA: 2004. pp. 1–28.
    1. Chaudhary K., Imam A.M., Rizvi S.Z.H., Ali J. Kinetic Theory. InTech; Rijeka, Croatia: 2018. Plasma Kinetic Theory; pp. 107–127.
    1. Sakudo A., Yagyu Y., Onodera T. Disinfection and Sterilization Using Plasma Technology: Fundamentals and Future Perspectives for Biological Applications. Int. J. Mol. Sci. 2019;20:5216. doi: 10.3390/ijms20205216.
    1. Conrads H., Schmidt M. Plasma Generation and Plasma Sources. Plasma Sources Sci. Technol. 2000;9:441. doi: 10.1088/0963-0252/9/4/301.
    1. Fridman G., Friedman G., Gutsol A., Shekhter A.B., Vasilets V.N., Fridman A. Applied Plasma Medicine. Plasma Process. Polym. 2008;5:503–533. doi: 10.1002/ppap.200700154.
    1. Fiebrandt M., Lackmann J.W., Stapelmann K. From Patent to Product? 50 Years of Low-Pressure Plasma Sterilization. Plasma Process. Polym. 2018;15:1800139. doi: 10.1002/ppap.201800139.
    1. Laroussi M. Plasma Medicine: A Brief Introduction. Plasma. 2018;1:47–60. doi: 10.3390/plasma1010005.
    1. Napp J., Daeschlein G., Napp M., von Podewils S., Gümbel D., Spitzmueller R., Fornaciari P., Hinz P., Jünger M. On the History of Plasma Treatment and Comparison of Microbiostatic Efficacy of a Historical High-Frequency Plasma Device with Two Modern Devices. GMS Hyg. Infect. Control. 2015;10:Doc08. doi: 10.3205/dgkh000251.
    1. Klämpfl T.G., Isbary G., Shimizu T., Li Y.F., Zimmermann J.L., Stolz W., Schlegel J., Morfill G.E., Schmidt H.U. Cold Atmospheric Air Plasma Sterilization against Spores and Other Microorganisms of Clinical Interest. Appl. Environ. Microbiol. 2012;78:5077–5082. doi: 10.1128/AEM.00583-12.
    1. Lu H., Patil S., Keener K.M., Cullen P.J., Bourke P. Bacterial Inactivation by High-Voltage Atmospheric Cold Plasma: Influence of Process Parameters and Effects on Cell Leakage and DNA. J. Appl. Microbiol. 2014;116:784–794. doi: 10.1111/jam.12426.
    1. Graves D.B. Reactive Species from Cold Atmospheric Plasma: Implications for Cancer Therapy. Plasma Process. Polym. 2014;11:1120–1127. doi: 10.1002/ppap.201400068.
    1. Yan D., Sherman J.H., Keidar M. Cold Atmospheric Plasma, a Novel Promising Anti-Cancer Treatment Modality. Oncotarget. 2017;8:15977–15995. doi: 10.18632/oncotarget.13304.
    1. Pai K., Timmons C., Roehm K.D., Ngo A., Narayanan S.S., Ramachandran A., Jacob J.D., Ma L.M., Madihally S.V. Investigation of the Roles of Plasma Species Generated by Surface Dielectric Barrier Discharge. Sci. Rep. 2018;8:1–13. doi: 10.1038/s41598-018-35166-0.
    1. Kim S.J., Chung T.H. Cold Atmospheric Plasma Jet-Generated RONS and Their Selective Effects on Normal and Carcinoma Cells. Sci. Rep. 2016;6:20332. doi: 10.1038/srep20332.
    1. Kalghatgi S., Kelly C.M., Cerchar E., Torabi B., Alekseev O., Fridman A., Friedman G., Azizkhan-Clifford J. Effects of Non-Thermal Plasma on Mammalian Cells. PLoS ONE. 2011;6:e16270. doi: 10.1371/journal.pone.0016270.
    1. Thiyagarajan M., Anderson H., Gonzales X.F. Induction of Apoptosis in Human Myeloid Leukemia Cells by Remote Exposure of Resistive Barrier Cold Plasma. Biotechnol. Bioeng. 2014;111:565–574. doi: 10.1002/bit.25114.
    1. Kim S.J., Chung T.H., Bae S.H., Leem S.H. Induction of Apoptosis in Human Breast Cancer Cells by a Pulsed Atmospheric Pressure Plasma Jet. Appl. Phys. Lett. 2010;97:023702. doi: 10.1063/1.3462293.
    1. Von Woedtke T., Schmidt A., Bekeschus S., Wende K., Weltmann K.D. Plasma Medicine: A Field of Applied Redox Biology. In Vivo. 2019;33:1011–1026. doi: 10.21873/invivo.11570.
    1. Takamatsu T., Uehara K., Sasaki Y., Miyahara H., Matsumura Y., Iwasawa A., Ito N., Azuma T., Kohno M., Okino A. Investigation of Reactive Species Using Various Gas Plasmas. RSC Adv. 2014;4:39901–39905. doi: 10.1039/C4RA05936K.
    1. Tanaka H., Nakamura K., Mizuno M., Ishikawa K., Takeda K., Kajiyama H., Utsumi F., Kikkawa F., Hori M. Non-Thermal Atmospheric Pressure Plasma Activates Lactate in Ringer’s Solution for Anti-Tumor Effects. Sci. Rep. 2016;6:1–11. doi: 10.1038/srep36282.
    1. Xiong Z. Plasma Medicine-Concepts and Clinical Applications. Volume 1. Intechopen; London, UK: 2018. Cold Atmospheric Pressure Plasmas (CAPs) for Skin Wound Healing; pp. 121–133.
    1. Von Woedtke T., Reuter S., Masur K., Weltmann K.D. Plasmas for Medicine. Phys. Rep. 2013;530:291–320. doi: 10.1016/j.physrep.2013.05.005.
    1. Keidar M., Shashurin A., Volotskova O., Stepp M.A., Srinivasan P., Homepage J., Sandler A., Trink B. Cold Atmospheric Plasma in Cancer Therapy Additional Information on Phys. Plasmas Cold Atmospheric Plasma in Cancer Therapy A) Cit. Phys. Plasmas. 2013;20:57101. doi: 10.1063/1.4801516.
    1. Nastuta A.V., Pohoata V., Topala I. Atmospheric Pressure Plasma Jet-Living Tissue Interface: Electrical, Optical, and Spectral Characterization. J. Appl. Phys. 2013;113:183302. doi: 10.1063/1.4804319.
    1. Gentile R.D. Cool Atmospheric Plasma (J-Plasma) and New Options for Facial Contouring and Skin Rejuvenation of the Heavy Face and Neck. Facial Plast. Surg. 2018;34:66–74. doi: 10.1055/s-0037-1621713.
    1. Chutsirimongkol C., Boonyawan D., Polnikorn N., Techawatthanawisan W., Kundilokchai T. Non-Thermal Plasma for Acne Treatment and Aesthetic Skin Improvement. Plasma Med. 2014;4:79–88. doi: 10.1615/PlasmaMed.2014011952.
    1. Bogle M.A., Arndt K.A., Dover J.S. Evaluation of Plasma Skin Regeneration Technology in Low-Energy Full-Facial Rejuvenation. Arch. Dermatol. 2007;143:168–174. doi: 10.1001/archderm.143.2.168.
    1. Isbary G., Shimizu T., Li Y.F., Stolz W., Thomas H.M., Morfill G.E., Zimmermann J.L. Cold Atmospheric Plasma Devices for Medical Issues. Expert Rev. Med. Devices. 2013;10:367–377. doi: 10.1586/erd.13.4.
    1. Hoffmann C., Berganza C., Zhang J. Cold Atmospheric Plasma: Methods of Production and Application in Dentistry and Oncology. Med. Gas Res. 2013;3:21. doi: 10.1186/2045-9912-3-21.
    1. Brandenburg R. Dielectric Barrier Discharges: Progress on Plasma Sources and on the Understanding of Regimes and Single Filaments. Plasma Sources Sci. Technol. 2017;26:053001. doi: 10.1088/1361-6595/aa6426.
    1. Zhang S., Chen Z., Zhang B., Chen Y. Numerical Investigation on the Effects of Dielectric Barrier on a Nanosecond Pulsed Surface Dielectric Barrier Discharge. Molecules. 2019;24:3933. doi: 10.3390/molecules24213933.
    1. Voráč J., Synek P., Procházka V., Hoder T. State-by-State Emission Spectra Fitting for Non-Equilibrium Plasmas: OH Spectra of Surface Barrier Discharge at Argon/Water Interface. J. Phys. D Appl. Phys. 2017;50:294002. doi: 10.1088/1361-6463/aa7570.
    1. Azzariti A., Iacobazzi R.M., Di Fonte R., Porcelli L., Gristina R., Favia P., Fracassi F., Trizio I., Silvestris N., Guida G., et al. Plasma-Activated Medium Triggers Cell Death and the Presentation of Immune Activating Danger Signals in Melanoma and Pancreatic Cancer Cells. Sci. Rep. 2019;9:1–13. doi: 10.1038/s41598-019-40637-z.
    1. Bauer G., Sersenová D., Graves D.B., Machala Z. Cold Atmospheric Plasma and Plasma-Activated Medium Trigger RONS-Based Tumor Cell Apoptosis. Sci. Rep. 2019;9:1–28. doi: 10.1038/s41598-019-50291-0.
    1. Kilmer S., Semchyshyn N., Shah G., Fitzpatrick R. A Pilot Study on the Use of a Plasma Skin Regeneration Device (Portrait® PSR3) in Full Facial Rejuvenation Procedures. Lasers Med. Sci. 2007;22:101–109. doi: 10.1007/s10103-006-0431-9.
    1. Isbary G., Morfill G., Schmidt H.U., Georgi M., Ramrath K., Heinlin J., Karrer S., Landthaler M., Shimizu T., Steffes B., et al. A First Prospective Randomized Controlled Trial to Decrease Bacterial Load Using Cold Atmospheric Argon Plasma on Chronic Wounds in Patients. Br. J. Dermatol. 2010;163:78–82. doi: 10.1111/j.1365-2133.2010.09744.x.
    1. Isbary G., Heinlin J., Shimizu T., Zimmermann J.L., Morfill G., Schmidt H.U., Monetti R., Steffes B., Bunk W., Li Y., et al. Successful and Safe Use of 2 Min Cold Atmospheric Argon Plasma in Chronic Wounds: Results of a Randomized Controlled Trial. Br. J. Dermatol. 2012;167:404–410. doi: 10.1111/j.1365-2133.2012.10923.x.
    1. Scotton M.F., Miot H.A., Abbade L.P.F. Factors That Influence Healing of Chronic Venous Leg Ulcers: A Retrospective Cohort. An. Bras. Dermatol. 2014;89:414–422. doi: 10.1590/abd1806-4841.20142687.
    1. Bevis P., Earnshaw J. Venous Ulcer RE. Clin. Cosmet. Investig. Dermatol. 2011;4:7–14. doi: 10.2147/CCID.S10171.
    1. Zmudzińska M., Czarnecka-Operacz M., Silny W. Analysis of Antibiotic Susceptibility and Resistance of Leg Ulcer Bacterial Flora in Patients Hospitalized at Dermatology Department, Poznań University Hospital. Acta Dermatovenerol. Croat. 2005;13:173–176.
    1. Rit K., Sarkar A., Maiti P., Nag F. Chronic Venous Leg Ulcer with Multidrug Resistant Bacterial Infection in a Tertiary Care Hospital of Eastern India. J. Sci. Soc. 2013;40:116. doi: 10.4103/0974-5009.115489.
    1. Brehmer F., Haenssle H.A., Daeschlein G., Ahmed R., Pfeiffer S., Görlitz A., Simon D., Schön M.P., Wandke D., Emmert S. Alleviation of Chronic Venous Leg Ulcers with a Hand-Held Dielectric Barrier Discharge Plasma Generator (PlasmaDerm ® VU-2010): Results of a Monocentric, Two-Armed, Open, Prospective, Randomized and Controlled Trial (NCT01415622) J. Eur. Acad. Dermatol. Venereol. 2015;29:148–155. doi: 10.1111/jdv.12490.
    1. Chuangsuwanich A., Assadamongkol T., Boonyawan D. The Healing Effect of Low-Temperature Atmospheric-Pressure Plasma in Pressure Ulcer: A Randomized Controlled Trial. Int. J. Low. Extrem. Wounds. 2016;15:313–319. doi: 10.1177/1534734616665046.
    1. Chatraie M., Torkaman G., Khani M., Salehi H., Shokri B. In Vivo Study of Non-Invasive Effects of Non-Thermal Plasma in Pressure Ulcer Treatment. Sci. Rep. 2018;8:1–11. doi: 10.1038/s41598-018-24049-z.
    1. Gao J., Wang L., Xia C., Yang X., Cao Z., Zheng L., Ko R., Shen C., Yang C., Cheng C. Cold Atmospheric Plasma Promotes Different Types of Superficial Skin Erosion Wounds Healing. Int. Wound J. 2019;16:1103–1111. doi: 10.1111/iwj.13161.
    1. Klebes M., Ulrich C., Kluschke F., Patzelt A., Vandersee S., Richter H., Bob A., von Hutten J., Krediet J.T., Kramer A., et al. Combined Antibacterial Effects of Tissue-Tolerable Plasma and a Modern Conventional Liquid Antiseptic on Chronic Wound Treatment. J. Biophotonics. 2015;8:382–391. doi: 10.1002/jbio.201400007.
    1. Ulrich C., Kluschke F., Patzelt A., Vandersee S., Czaika V.A., Richter H., Bob A., Von Hutten J., Painsi C., Hügel R., et al. Clinical Use of Cold Atmospheric Pressure Argon Plasma in Chronic Leg Ulcers: A Pilot Study. J. Wound Care. 2015;24:196–203. doi: 10.12968/jowc.2015.24.5.196.
    1. Schmidt A., Bekeschus S., Wende K., Vollmar B., von Woedtke T. A Cold Plasma Jet Accelerates Wound Healing in a Murine Model of Full-Thickness Skin Wounds. Exp. Dermatol. 2017;26:156–162. doi: 10.1111/exd.13156.
    1. Haertel B., Wende K., Von Woedtke T., Weltmann K.D., Lindequist U. Non-Thermal Atmospheric-Pressure Plasma Can Influence Cell Adhesion Molecules on HaCaT-Keratinocytes. Exp. Dermatol. 2011;20:282–284. doi: 10.1111/j.1600-0625.2010.01159.x.
    1. Schmidt A., Von Woedtke T., Sander B. Periodic Exposure of Keratinocytes to Cold Physical Plasma: An In Vitro Model for Redox-Related Diseases of the Skin. Oxidative Med. Cell. Longev. 2016;2016:1–17. doi: 10.1155/2016/9816072.
    1. Schmidt A., Bekeschus S., Jarick K., Hasse S., Von Woedtke T., Wende K. Cold Physical Plasma Modulates P53 and Mitogen-Activated Protein Kinase Signaling in Keratinocytes. Oxid. Med. Cell. Longev. 2019;2019:1–16. doi: 10.1155/2019/7017363.
    1. Shome D., von Woedtke T., Riedel K., Masur K. The HIPPO Transducer YAP and Its Targets CTGF and Cyr61 Drive a Paracrine Signalling in Cold Atmospheric Plasma-Mediated Wound Healing. Oxid. Med. Cell. Longev. 2020;2020:1–14. doi: 10.1155/2020/4910280.
    1. Zhao B., Ye X., Yu J., Li L., Li W., Li S., Yu J., Lin J.D., Wang C.Y., Chinnaiyan A.M., et al. TEAD Mediates YAP-Dependent Gene Induction and Growth Control. Genes Dev. 2008;22:1962–1971. doi: 10.1101/gad.1664408.
    1. Duchesne C., Banzet S., Lataillade J., Rousseau A., Frescaline N. Cold Atmospheric Plasma Modulates Endothelial Nitric Oxide Synthase Signalling and Enhances Burn Wound Neovascularisation. J. Pathol. 2019;249:368–380. doi: 10.1002/path.5323.
    1. Lee O.J., Ju H.W., Khang G., Sun P.P., Rivera J., Cho J.H., Park S.J., Eden J.G., Park C.H. An Experimental Burn Wound-Healing Study of Non-Thermal Atmospheric Pressure Microplasma Jet Arrays. J. Tissue Eng. Regen. Med. 2016;10:348–357. doi: 10.1002/term.2074.
    1. Ngo Thi M.H., Shao P.L., Der Liao J., Lin C.C.K., Yip H.K. Enhancement of Angiogenesis and Epithelialization Processes in Mice with Burn Wounds through ROS/RNS Signals Generated by Non-Thermal N2/Ar Micro-Plasma. Plasma Process. Polym. 2014;11:1076–1088. doi: 10.1002/ppap.201400072.
    1. Nastuta A.V., Pohoata V., Vasile Nastuta A., Topala I., Grigoras C., Popa G. Stimulation of Wound Healing by Helium Atmospheric Pressure Plasma Treatment. Artic. J. Phys. D Appl. Phys. 2011;44:105204–105213. doi: 10.1088/0022-3727/44/10/105204.
    1. Topala I., Nastuta A. NATO Science for Peace and Security Series A: Chemistry and Biology. Springer; Dordrecht, The Netherlands: 2012. Helium Atmospheric Pressure Plasma Jet: Diagnostics and Application for Burned Wounds Healing; pp. 335–345.
    1. Betancourt-Ángeles M., Peña-Eguiluz R., López-Callejas R., Domínguez-Cadena N.A., Mercado-Cabrera A., Muñoz-Infante J., Rodríguez-Méndez B.G., Valencia-Alvarado R., Moreno-Tapia J.A. Treatment in the Healing of Burns with a Cold Plasma Source. Int. J. Burns Trauma. 2017;7:142–146.
    1. Heinlin J., Zimmermann J.L., Zeman F., Bunk W., Isbary G., Landthaler M., Maisch T., Monetti R., Morfill G., Shimizu T., et al. Randomized Placebo-Controlled Human Pilot Study of Cold Atmospheric Argon Plasma on Skin Graft Donor Sites. Wound Repair Regen. 2013;21:800–807. doi: 10.1111/wrr.12078.
    1. Winter S., Meyer-Lindenberg A., Wolf G., Reese S., Nolff M.C. In Vitro Evaluation of the Decontamination Effect of Cold Atmospheric Argon Plasma on Selected Bacteria Frequently Encountered in Small Animal Bite Injuries. J. Microbiol. Methods. 2020;169:105728. doi: 10.1016/j.mimet.2019.105728.
    1. Winter S., Nolff M., Reese S., Meyer-Lindenberg A. Vergleich Der Effizienz von Polyhexanid-Biguanid, Argon-Kaltplasma Und Kochsalzlavage Zur Dekontamination von Bisswunden Beim Hund. Tierärztliche Prax. Ausgabe K Kleintiere / Heimtiere. 2018;46:73–82. doi: 10.15654/TPK-170713.
    1. Metelmann H.R., Vu T.T., Do H.T., Le T.N.B., Hoang T.H.A., Phi T.T.T., Luong T.M.L., Doan V.T., Nguyen T.T.H., Nguyen T.H.M., et al. Scar Formation of Laser Skin Lesions after Cold Atmospheric Pressure Plasma (CAP) Treatment: A Clinical Long Term Observation. Clin. Plasma Med. 2013;1:30–35. doi: 10.1016/j.cpme.2012.12.001.
    1. Nishijima A., Fujimoto T., Hirata T., Nishijima J. Effects of Cold Atmospheric Pressure Plasma on Accelerating Acute Wound Healing: A Comparative Study among 4 Different Treatment Groups. Mod. Plast. Surg. 2019;9:18–31. doi: 10.4236/mps.2019.91004.
    1. Ranjan R., Krishnamraju P.V., Shankar T., Gowd S. Nonthermal Plasma in Dentistry: An Update. J. Int. Soc. Prev. Community Dent. 2017;7:71–75. doi: 10.4103/jispcd.JISPCD_29_17.
    1. Pan J., Sun K., Liang Y., Sun P., Yang X., Wang J., Zhang J., Zhu W., Fang J., Becker K.H. Cold Plasma Therapy of a Tooth Root Canal Infected with Enterococcus Faecalis Biofilms in Vitro. J. Endod. 2013;39:105–110. doi: 10.1016/j.joen.2012.08.017.
    1. Vandana B.L. From Distant Stars to Dental Chairs: An Update on Plasma Needle. Int. J. Dent. Sci. Res. 2014;2:19–20. doi: 10.12691/ijdsr-2-6B-6.
    1. Aparecida Delben J., Evelin Zago C., Tyhovych N., Duarte S., Eduardo Vergani C. Effect of Atmospheric-Pressure Cold Plasma on Pathogenic Oral Biofilms and in Vitro Reconstituted Oral Epithelium. PLoS ONE. 2016;11:e0155427.
    1. Marsh P.D., Zaura E. Dental Biofilm: Ecological Interactions in Health and Disease. J. Clin. Periodontol. 2017;44:S12–S22. doi: 10.1111/jcpe.12679.
    1. Koban I., Holtfreter B., Hübner N.O., Matthes R., Sietmann R., Kindel E., Weltmann K.D., Welk A., Kramer A., Kocher T. 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. 2011;38:956–965. doi: 10.1111/j.1600-051X.2011.01740.x.
    1. Jiang C., Chen M.-T., Gorur A., Schaudinn C., Jaramillo D.E., Costerton J.W., Sedghizadeh P.P., Vernier P.T., Gundersen M.A. Nanosecond Pulsed Plasma Dental Probe. Plasma Process. Polym. 2009;6:479–483. doi: 10.1002/ppap.200800133.
    1. Armand A., Khani M., Asnaashari M., AliAhmadi A., Shokri B. Comparison Study of Root Canal Disinfection by Cold Plasma Jet and Photodynamic Therapy. Photodiagnosis Photodyn. Ther. 2019;26:327–333. doi: 10.1016/j.pdpdt.2019.04.023.
    1. Wang Q.Q., Zhang C.F., Chu C.H., Zhu X.F. Prevalence of Enterococcus Faecalis in Saliva and Filled Root Canals of Teeth Associated with Apical Periodontitis. Int. J. Oral Sci. 2012;4:19–23. doi: 10.1038/ijos.2012.17.
    1. Shahmohammadi Beni M., Han W., Yu K.N. Dispersion of OH Radicals in Applications Related to Fear-Free Dentistry Using Cold Plasma. Appl. Sci. 2019;9:2119. doi: 10.3390/app9102119.
    1. Dong X., Chen M., Wang Y., Yu Q. A Mechanistic Study of Plasma Treatment Effects on Demineralized Dentin Surfaces for Improved Adhesive/Dentin Interface Bonding. Clin. Plasma Med. 2014;2:11–16. doi: 10.1016/j.cpme.2014.04.001.
    1. Yavirach P., Chaijareenont P., Boonyawan D., Pattamapun K., Tunma S., Takahashi H., Arksornnukit M. Effects of Plasma Treatment on the Shear Bond Strength between Fiberreinforced Composite Posts and Resin Composite for Core Build-Up. Dent. Mater. J. 2009;28:686–692. doi: 10.4012/dmj.28.686.
    1. Yang Y., Guo J., Zhou X., Liu Z., Wang C., Wang K., Zhang J., Wang Z. A Novel Cold Atmospheric Pressure Air Plasma Jet for Peri-Implantitis Treatment: An in Vitro Study. Dent. Mater. J. 2018;37:157–166. doi: 10.4012/dmj.2017-030.
    1. Monetto I. The Effects of an Interlayer Debond on the Flexural Behavior of Three-Layer Beams. Coatings. 2019;9:258. doi: 10.3390/coatings9040258.
    1. Quirynen M., Bollen C.M.L. CA Novel Cold Atmospheric Pressure Air Plasma Jet for Peri-Implantitis Treatment: An in Vitro Study. J. Clin. Periodontol. 1995;22:1–14. doi: 10.1111/j.1600-051X.1995.tb01765.x.
    1. Yang Y., Zheng M., Yang Y., Li J., Su Y.F., Li H.P., Tan J.G. Inhibition of Bacterial Growth on Zirconia Abutment with a Helium Cold Atmospheric Plasma Jet Treatment. Clin. Oral Investig. 2020:1–13. doi: 10.1007/s00784-019-03179-2.
    1. Preissner S., Poehlmann A.C., Schubert A., Lehmann A., Arnold T., Nell O., Rupf S. Ex Vivo Study Comparing Three Cold Atmospheric Plasma (CAP) Sources for Ebiofllmeremovaleonemicrostructuredetitanium. Plasma Med. 2019;9:1–13. doi: 10.1615/PlasmaMed.2018027314.
    1. Park J., Lee H., Lee H.J., Kim G.C., Kim D.Y., Han S., Song K. Non-Thermal Atmospheric Pressure Plasma Efficiently Promotes the Proliferation of Adipose Tissue-Derived Stem Cells by Activating NO-Response Pathways. Sci. Rep. 2016;6:1–12. doi: 10.1038/srep39298.
    1. Elsaadany M., Subramanian G., Ayan H., Yildirim-Ayan E. Exogenous Nitric Oxide (NO) Generated by NO-Plasma Treatment Modulates Osteoprogenitor Cells Early Differentiation. J. Phys. D Appl. Phys. 2015;48:345401. doi: 10.1088/0022-3727/48/34/345401.
    1. Han I., Choi E.H. The Role of Non-Thermal Atmospheric Pressure Biocompatible Plasma in the Differentiation of Osteoblastic Precursor Cells, MC3T3-E1. Oncotarget. 2017;8:36399. doi: 10.18632/oncotarget.16821.
    1. Klotz L.O., Sánchez-Ramos C., Prieto-Arroyo I., Urbánek P., Steinbrenner H., Monsalve M. Redox Regulation of FoxO Transcription Factors. Redox Biol. 2015;6:51–72. doi: 10.1016/j.redox.2015.06.019.
    1. Miletić M., Mojsilović S., Okićorević I., Maletić D., Puač N., Lazović S., Malović G., Milenković P., Lj Petrović Z., Bugarski D. Effects of Non-Thermal Atmospheric Plasma on Human Periodontal Ligament Mesenchymal Stem Cells. J. Phys. D Appl. Phys. 2013;46:345401–345410. doi: 10.1088/0022-3727/46/34/345401.
    1. Park J., Lee H., Lee H.J., Kim G.C., Kim S.S., Han S., Song K. Non-Thermal Atmospheric Pressure Plasma Is an Excellent Tool to Activate Proliferation in Various Mesoderm-Derived Human Adult Stem Cells. Free Radic. Biol. Med. 2019;134:374–384. doi: 10.1016/j.freeradbiomed.2019.01.032.
    1. Alemi P.S., Atyabi S.A., Sharifi F., Mohamadali M., Irani S., Bakhshi H., Atyabi S.M. Synergistic Effect of Pressure Cold Atmospheric Plasma and Carboxymethyl Chitosan to Mesenchymal Stem Cell Differentiation on PCL/CMC Nanofibers for Cartilage Tissue Engineering. Polym. Adv. Technol. 2019;30:1356–1364. doi: 10.1002/pat.4568.
    1. Xiong Z., Zhao S., Yan X. Nerve Stem Cell Differentiation by a One-Step Cold Atmospheric Plasma Treatment in Vitro. J. Vis. Exp. 2019;2019:e58663. doi: 10.3791/58663.
    1. Jouhilahti E.M., Peltonen S., Peltonen J. Class III β-Tubulin Is a Component of the Mitotic Spindle in Multiple Cell Types. J. Histochem. Cytochem. 2008;56:1113–1119. doi: 10.1369/jhc.2008.952002.
    1. Foudah D., Monfrini M., Donzelli E., Niada S., Brini A.T., Orciani M., Tredici G., Miloso M. Expression of Neural Markers by Undifferentiated Mesenchymal-like Stem Cells from Different Sources. J. Immunol. Res. 2014;2014:1–16. doi: 10.1155/2014/987678.
    1. Weil M.T., Schulz-Ëberlin G., Mukherjee C., Kuo-Elsner W.P., Schäfer I., Müller C., Simons M. Methods in Molecular Biology. Volume 1936. Humana Press Inc.; Totowa, NJ, USA: 2019. Isolation and Culture of Oligodendrocytes; pp. 79–95.
    1. Hol E.M., Pekny M. Glial Fibrillary Acidic Protein (GFAP) and the Astrocyte Intermediate Filament System in Diseases of the Central Nervous System. Curr. Opin. Cell Biol. 2015;32:121–130. doi: 10.1016/j.ceb.2015.02.004.
    1. Jang J.Y., Hong Y.J., Lim J., Choi J.S., Choi E.H., Kang S., Rhim H. Cold Atmospheric Plasma (CAP), a Novel Physicochemical Source, Induces Neural Differentiation through Cross-Talk between the Specific RONS Cascade and Trk/Ras/ERK Signaling Pathway. Biomaterials. 2018;156:258–273. doi: 10.1016/j.biomaterials.2017.11.045.
    1. Bourdens M., Jeanson Y., Taurand M., Juin N., Carrière A., Clément F., Casteilla L., Bulteau A.L., Planat-Bénard V. Short Exposure to Cold Atmospheric Plasma Induces Senescence in Human Skin Fibroblasts and Adipose Mesenchymal Stromal Cells. Sci. Rep. 2019;9:1–15. doi: 10.1038/s41598-019-45191-2.
    1. Won H.-R., Kang S.U., Kim H.J., Jang J.Y., Shin Y.S., Kim C.-H. Non-Thermal Plasma Treated Solution with Potential as a Novel Therapeutic Agent for Nasal Mucosa Regeneration. Sci. Rep. 2018;8:13754. doi: 10.1038/s41598-018-32077-y.
    1. Scharf C., Eymann C., Emicke P., Bernhardt J., Wilhelm M., Görries F., Winter J., Von Woedtke T., Darm K., Daeschlein G., et al. Improved Wound Healing of Airway Epithelial Cells Is Mediated by Cold Atmospheric Plasma: A Time Course-Related Proteome Analysis. Hindawi Oxidative Med. Cell. Longev. 2019;2019:1–21. doi: 10.1155/2019/7071536.
    1. Katiyar K.S., Lin A., Fridman A., Keating C.E., Cullen D.K., Miller V. Non-Thermal Plasma Accelerates Astrocyte Regrowth and Neurite Regeneration Following Physical Trauma in Vitro. Appl. Sci. 2019;9:3747. doi: 10.3390/app9183747.
    1. Aggarwal V., Tuli H.S., Varol A., Thakral F., Yerer M.B., Sak K., Varol M., Jain A., Khan M.A., Sethi G. Role of Reactive Oxygen Species in Cancer Progression: Molecular Mechanisms and Recent Advancements. Biomolecules. 2019;9:735. doi: 10.3390/biom9110735.
    1. Aikman B., De Almeida A., Meier-Menches S.M., Casini A. Aquaporins in Cancer Development: Opportunities for Bioinorganic Chemistry to Contribute Novel Chemical Probes and Therapeutic Agents. Metallomics. 2018;10:696–712. doi: 10.1039/C8MT00072G.
    1. Yusupov M., Razzokov J., Cordeiro R.M., Bogaerts A. Transport of Reactive Oxygen and Nitrogen Species across Aquaporin: A Molecular Level Picture. Oxid. Med. Cell. Longev. 2019;2019:1–11. doi: 10.1155/2019/2930504.
    1. Tamma G., Valenti G., Grossini E., Donnini S., Marino A., Marinelli R.A., Calamita G. Aquaporin Membrane Channels in Oxidative Stress, Cell Signaling, and Aging: Recent Advances and Research Trends. Oxidative Med. Cell. Longev. 2018;2018:1–14. doi: 10.1155/2018/1501847.
    1. Rivel T., Ramseyer C., Yesylevskyy S. The Asymmetry of Plasma Membranes and Their Cholesterol Content Influence the Uptake of Cisplatin. Sci. Rep. 2019;9:1–14. doi: 10.1038/s41598-019-41903-w.
    1. Van Der Paal J., Neyts E.C., Verlackt C.C.W., Bogaerts A. Effect of Lipid Peroxidation on Membrane Permeability of Cancer and Normal Cells Subjected to Oxidative Stress. Chem. Sci. 2016;7:489–498. doi: 10.1039/C5SC02311D.
    1. Keidar M., Yan D., Beilis I.I., Trink B., Sherman J.H. Plasmas for Treating Cancer: Opportunities for Adaptive and Self-Adaptive Approaches. Trends Biotechnol. 2018;36:586–593. doi: 10.1016/j.tibtech.2017.06.013.
    1. Yan D., Talbot A., Nourmohammadi N., Cheng X., Canady J., Sherman J., Keidar M. Principles of Using Cold Atmospheric Plasma Stimulated Media for Cancer Treatment. Sci. Rep. 2015;5:1–17. doi: 10.1038/srep18339.
    1. Siu A., Volotskova O., Cheng X., Khalsa S.S., Bian K., Murad F., Keidar M., Sherman J.H. Differential Effects of Cold Atmospheric Plasma in the Treatment of Malignant Glioma. PLoS ONE. 2015;10:e0126313. doi: 10.1371/journal.pone.0126313.
    1. Wiegand C., Fink S., Beier O., Horn K., Pfuch A., Schimanski A., Grünler B., Hipler U.-C., Elsner P. Dose- and Time-Dependent Cellular Effects of Cold Atmospheric Pressure Plasma Evaluated in 3D Skin Models. Skin Pharmacol. Physiol. 2016;29:257–265. doi: 10.1159/000450889.
    1. Keidar M., Walk R., Shashurin A., Srinivasan P., Sandler A., Dasgupta S., Ravi R., Guerrero-Preston R., Trink B. Cold Plasma Selectivity and the Possibility of a Paradigm Shift in Cancer Therapy. Br. J. Cancer. 2011;105:1295–1301. doi: 10.1038/bjc.2011.386.
    1. Kaushik N., Uddin N., Sim G.B., Hong Y.J., Baik K.Y., Kim C.H., Lee S.J., Kaushik N.K., Choi E.H. Responses of Solid Tumor Cells in DMEM to Reactive Oxygen Species Generated by Non-Thermal Plasma and Chemically Induced ROS Systems. Sci. Rep. 2015;5:8587. doi: 10.1038/srep08587.
    1. DeBerardinis R.J., Lum J.J., Hatzivassiliou G., Thompson C.B. The Biology of Cancer: Metabolic Reprogramming Fuels Cell Growth and Proliferation. Cell Metab. 2008;7:11–20. doi: 10.1016/j.cmet.2007.10.002.
    1. Cha J.-Y., Lee H.-J. Targeting Lipid Metabolic Reprogramming as Anticancer Therapeutics. J. Cancer Prev. 2016;21:209–215. doi: 10.15430/JCP.2016.21.4.209.
    1. Ward P.S., Thompson C.B. Metabolic Reprogramming: A Cancer Hallmark Even Warburg Did Not Anticipate. Cancer Cell. 2012;21:297–308. doi: 10.1016/j.ccr.2012.02.014.
    1. Xu D., Ning N., Xu Y., Wang B., Cui Q., Liu Z., Wang X., Liu D., Chen H., Kong M.G. Effect of Cold Atmospheric Plasma Treatment on the Metabolites of Human Leukemia Cells. Cancer Cell Int. 2019;19:135. doi: 10.1186/s12935-019-0856-4.
    1. Köritzer J., Boxhammer V., Schäfer A., Shimizu T., Klämpfl T.G., Li Y.-F., Welz C., Schwenk-Zieger S., Morfill G.E., Zimmermann J.L., et al. Restoration of Sensitivity in Chemo—Resistant Glioma Cells by Cold Atmospheric Plasma. PLoS ONE. 2013;8:e64498. doi: 10.1371/journal.pone.0064498.
    1. Vandamme M., Robert E., Lerondel S., Sarron V., Ries D., Dozias S., Sobilo J., Gosset D., Kieda C., Legrain B., et al. ROS Implication in a New Antitumor Strategy Based on Non-Thermal Plasma. Int. J. Cancer. 2012;130:2185–2194. doi: 10.1002/ijc.26252.
    1. Tanaka H., Mizuno M., Ishikawa K., Nakamura K., Kajiyama H., Kano H., Kikkawa F., Hori M. Plasma-Activated Medium Selectively Kills Glioblastoma Brain Tumor Cells by Down-Regulating a Survival Signaling Molecule, AKT Kinase. Plasma Med. 2011;1:265–277. doi: 10.1615/PlasmaMed.2012006275.
    1. Kaushik N.K., Attri P., Kaushik N., Choi E.H. A Preliminary Study of the Effect of DBD Plasma and Osmolytes on T98G Brain Cancer and HEK Non-Malignant Cells. Molecules. 2013;18:4917–4928. doi: 10.3390/molecules18054917.
    1. Kim J.Y., Ballato J., Foy P., Hawkins T., Wei Y., Li J., Kim S.O. Apoptosis of Lung Carcinoma Cells Induced by a Flexible Optical Fiber-Based Cold Microplasma. Biosens. Bioelectron. 2011;28:333–338. doi: 10.1016/j.bios.2011.07.039.
    1. Chen Z., Simonyan H., Cheng X., Gjika E., Lin L., Canady J., Sherman J.H., Young C., Keidar M. A Novel Micro Cold Atmospheric Plasma Device for Glioblastoma both in Vitro and in Vivo. Cancers. 2017;9:61. doi: 10.3390/cancers9060061.
    1. Chen Z., Lin L., Zheng Q., Sherman J.H., Canady J., Trink B., Keidar M. Micro-Sized Cold Atmospheric Plasma Source for Brain and Breast Cancer Treatment. Plasma Med. 2018;8:203–215. doi: 10.1615/PlasmaMed.2018026588.
    1. Mirpour S., Piroozmand S., Soleimani N., Jalali Faharani N., Ghomi H., Fotovat Eskandari H., Sharifi A.M., Mirpour S., Eftekhari M., Nikkhah M. Utilizing the Micron Sized Non-Thermal Atmospheric Pressure Plasma inside the Animal Body for the Tumor Treatment Application. Sci. Rep. 2016;6:29048. doi: 10.1038/srep29048.
    1. Mashayekh S., Rajaee H., Akhlaghi M., Shokri B., Hassan Z.M. Atmospheric-Pressure Plasma Jet Characterization and Applications on Melanoma Cancer Treatment (B/16-F10) Phys. Plasmas. 2015;22:093508. doi: 10.1063/1.4930536.
    1. Lee H.J., Shon C.H., Kim Y.S., Kim S., Kim G.C., Kong M.G. Degradation of Adhesion Molecules of G361 Melanoma Cells by a Non-Thermal Atmospheric Pressure Microplasma. New J. Phys. 2009;11:115026. doi: 10.1088/1367-2630/11/11/115026.
    1. Kim G.C., Kim G.J., Park S.R., Jeon S.M., Seo H.J., Iza F., Lee J.K. Air Plasma Coupled with Antibody-Conjugated Nanoparticles: A New Weapon against Cancer. J. Phys. D Appl. Phys. 2009;42:032005. doi: 10.1088/0022-3727/42/3/032005.
    1. Ninomiya K., Ishijima T., Imamura M., Yamahara T., Enomoto H., Takahashi K., Tanaka Y., Uesugi Y., Shimizu N. Evaluation of Extra- and Intracellular OH Radical Generation, Cancer Cell Injury, and Apoptosis Induced by a Non-Thermal Atmospheric-Pressure Plasma Jet. J. Phys. D Appl. Phys. 2013;46:425401. doi: 10.1088/0022-3727/46/42/425401.
    1. Kim C.H., Bahn J.H., Lee S.H., Kim G.Y., Jun S.I., Lee K., Baek S.J. Induction of Cell Growth Arrest by Atmospheric Non-Thermal Plasma in Colorectal Cancer Cells. J. Biotechnol. 2010;150:530–538. doi: 10.1016/j.jbiotec.2010.10.003.
    1. Georgescu N., Lupu A.R. Tumoral and Normal Cells Treatment with High-Voltage Pulsed Cold Atmospheric Plasma Jets. IEEE Trans. Plasma Sci. 2010;38:1949–1955. doi: 10.1109/TPS.2010.2041075.
    1. Ishaq M., Evans M.D.M., Ostrikov K.K. Atmospheric Pressure Gas Plasma-Induced Colorectal Cancer Cell Death Is Mediated by Nox2-ASK1 Apoptosis Pathways and Oxidative Stress Is Mitigated by Srx-Nrf2 Anti-Oxidant System. Biochim. Biophys. Acta-Mol. Cell Res. 2014;1843:2827–2837. doi: 10.1016/j.bbamcr.2014.08.011.
    1. Plewa J.M., Yousfi M., Frongia C., Eichwald O., Ducommun B., Merbahi N., Lobjois V. Low-Temperature Plasma-Induced Antiproliferative Effects on Multi-Cellular Tumor Spheroids. New J. Phys. 2014;16:043027. doi: 10.1088/1367-2630/16/4/043027.
    1. Guerrero-Preston R., Ogawa T., Uemura M., Shumulinsky G., Valle B.L., Pirini F., Ravi R., Sidransky D., Keidar M., Trink B. Cold Atmospheric Plasma Treatment Selectively Targets Head and Neck Squamous Cell Carcinoma Cells. Int. J. Mol. Med. 2014;34:941–946. doi: 10.3892/ijmm.2014.1849.
    1. Kang S.U., Cho J.H., Chang J.W., Shin Y.S., Kim K.I., Park J.K., Yang S.S., Lee J.S., Moon E., Lee K., et al. Nonthermal Plasma Induces Head and Neck Cancer Cell Death: The Potential Involvement of Mitogen-Activated Protein Kinase-Dependent Mitochondrial Reactive Oxygen Species. Cell Death Dis. 2014;5:e1056. doi: 10.1038/cddis.2014.33.
    1. Hasse S., Seebauer C., Wende K., Schmidt A., Metelmann H.-R., von Woedtke T., Bekeschus S. Cold Argon Plasma as Adjuvant Tumour Therapy on Progressive Head and Neck Cancer: A Preclinical Study. Appl. Sci. 2019;9:2061. doi: 10.3390/app9102061.
    1. Ahn H.J., Kim K., II, Hoan N.N., Kim C.H., Moon E., Choi K.S., Yang S.S., Lee J.S. Targeting Cancer Cells with Reactive Oxygen and Nitrogen Species Generated by Atmospheric-Pressure Air Plasma. PLoS ONE. 2014;9:e86173. doi: 10.1371/journal.pone.0086173.
    1. Kim K., Jun Ahn H., Lee J.H., Kim J.H., Sik Yang S., Lee J.S. Cellular Membrane Collapse by Atmospheric-Pressure Plasma Jet. Appl. Phys. Lett. 2014;104:013701. doi: 10.1063/1.4861373.
    1. Tan X., Zhao S., Lei Q., Lu X., He G., Ostrikov K. Single-Cell-Precision Microplasma-Induced Cancer Cell Apoptosis. PLoS ONE. 2014;9:e101299. doi: 10.1371/journal.pone.0101299.
    1. Barekzi N., Laroussi M. Dose-Dependent Killing of Leukemia Cells by Low-Temperature Plasma. J. Phys. D Appl. Phys. 2012;45:422002. doi: 10.1088/0022-3727/45/42/422002.
    1. Thiyagarajan M., Waldbeser L., Whitmill A. THP-1 Leukemia Cancer Treatment Using a Portable Plasma Device. Stud. Health Technol. Inform. 2012;173:515–517. doi: 10.3233/978-1-61499-022-2-515.
    1. Brullé L., Vandamme M., Riès D., Martel E., Robert E., Lerondel S., Trichet V., Richard S., Pouvesle J.M., Le Pape A. Effects of a Non Thermal Plasma Treatment Alone or in Combination with Gemcitabine in a MIA PaCa2-Luc Orthotopic Pancreatic Carcinoma Model. PLoS ONE. 2012;7:e52653. doi: 10.1371/journal.pone.0052653.
    1. Hattori N., Yamada S., Tori K., Takeda S., Nakamura K., Tanaka H., Kajiyama H., Kanda M., Fuji T., Nakayama G., et al. Effectiveness of Plasma Treatment on Pancreatic Cancer Cells. Int. J. Oncol. 2015;47:1655–1662. doi: 10.3892/ijo.2015.3149.
    1. Metelmann H.R., Seebauer C., Miller V., Fridman A., Bauer G., Graves D.B., Pouvesle J.M., Rutkowski R., Schuster M., Bekeschus S., et al. Clinical Experience with Cold Plasma in the Treatment of Locally Advanced Head and Neck Cancer. Clin. Plasma Med. 2018;9:6–13. doi: 10.1016/j.cpme.2017.09.001.
    1. Tanaka H., Mizuno M., Ishikawa K., Toyokuni S., Kajiyama H., Kikkawa F., Hori M. New Hopes for Plasma-Based Cancer Treatment. Plasma. 2018;1:150–155. doi: 10.3390/plasma1010014.
    1. Yan D., Xiao H., Zhu W., Nourmohammadi N., Zhang L.G., Bian K., Keidar M. The Role of Aquaporins in the Anti-Glioblastoma Capacity of the Cold Plasma-Stimulated Medium. J. Phys. D Appl. Phys. 2017;50:055401. doi: 10.1088/1361-6463/aa53d6.
    1. Torii K., Yamada S., Nakamura K., Tanaka H., Kajiyama H., Tanahashi K., Iwata N., Kanda M., Kobayashi D., Tanaka C., et al. Effectiveness of Plasma Treatment on Gastric Cancer Cells. Gastric Cancer. 2015;18:635–643. doi: 10.1007/s10120-014-0395-6.
    1. Ishimoto T., Nagano O., Yae T., Tamada M., Motohara T., Oshima H., Oshima M., Ikeda T., Asaba R., Yagi H., et al. CD44 Variant Regulates Redox Status in Cancer Cells by Stabilizing the XCT Subunit of System Xc- and Thereby Promotes Tumor Growth. Cancer Cell. 2011;19:387–400. doi: 10.1016/j.ccr.2011.01.038.
    1. Utsumi F., Kajiyama H., Nakamura K., Tanaka H., Mizuno M., Ishikawa K., Kondo H., Kano H., Hori M., Kikkawa F. Effect of Indirect Nonequilibrium Atmospheric Pressure Plasma on Anti-Proliferative Activity against Chronic Chemo-Resistant Ovarian Cancer Cells In Vitro and In Vivo. PLoS ONE. 2013;8:e81576. doi: 10.1371/journal.pone.0081576.
    1. Nakamura K., Peng Y., Utsumi F., Tanaka H., Mizuno M., Toyokuni S., Hori M., Kikkawa F., Kajiyama H. Novel Intraperitoneal Treatment with Non-Thermal Plasma-Activated Medium Inhibits Metastatic Potential of Ovarian Cancer Cells. Sci. Rep. 2017;7:1–14. doi: 10.1038/s41598-017-05620-6.
    1. Sato Y., Yamada S., Takeda S., Hattori N., Nakamura K., Tanaka H., Mizuno M., Hori M., Kodera Y. Effect of Plasma-Activated Lactated Ringer’s Solution on Pancreatic Cancer Cells In Vitro and In Vivo. Ann. Surg. Oncol. 2018;25:299–307. doi: 10.1245/s10434-017-6239-y.
    1. Matsuzaki T., Kano A., Kamiya T., Hara H., Adachi T. Enhanced Ability of Plasma-Activated Lactated Ringer’s Solution to Induce A549 cell Injury. Arch. Biochem. Biophys. 2018;656:19–30. doi: 10.1016/j.abb.2018.08.011.
    1. Chen D.S., Mellman I. Elements of Cancer Immunity and the Cancer-Immune Set Point. Nature. 2017;541:321–330. doi: 10.1038/nature21349.
    1. Radogna F., Diederich M. Stress-Induced Cellular Responses in Immunogenic Cell Death: Implications for Cancer Immunotherapy. Biochem. Pharmacol. 2018;153:12–23. doi: 10.1016/j.bcp.2018.02.006.
    1. Hernandez C., Huebener P., Schwabe R.F. Damage-Associated Molecular Patterns in Cancer: A Double-Edged Sword. Oncogene. 2016;35:5931–5941. doi: 10.1038/onc.2016.104.
    1. Lin A.G., Xiang B., Merlino D.J., Baybutt T.R., Sahu J., Fridman A., Snook A.E., Miller V. Non-Thermal Plasma Induces Immunogenic Cell Death in Vivo in Murine CT26 Colorectal Tumors. Oncoimmunology. 2018;7:e1484978. doi: 10.1080/2162402X.2018.1484978.
    1. Khalili M., Daniels L., Lin A., Krebs F.C., Snook A.E., Bekeschus S., Bowne W.B., Miller V. Non-Thermal Plasma-Induced Immunogenic Cell Death in Cancer. J. Phys. D Appl. Phys. 2019;52:423001. doi: 10.1088/1361-6463/ab31c1.
    1. Miller V., Lin A., Fridman A. Why Target Immune Cells for Plasma Treatment of Cancer. Plasma Chem. Plasma Process. 2016;36:259–268. doi: 10.1007/s11090-015-9676-z.
    1. Almeida N.D., Klein A.L., Hogan E.A., Terhaar S.J., Kedda J., Uppal P., Sack K., Keidar M., Sherman J.H. Cold Atmospheric Plasma as an Adjunct to Immunotherapy for Glioblastoma Multiforme. World Neurosurg. 2019;130:369–376. doi: 10.1016/j.wneu.2019.06.209.
    1. Lin A., Truong B., Patel S., Kaushik N., Choi E.H., Fridman G., Fridman A., Miller V. Nanosecond-Pulsed DBD Plasma-Generated Reactive Oxygen Species Trigger Immunogenic Cell Death in A549 Lung Carcinoma Cells through Intracellular Oxidative Stress. Int. J. Mol. Sci. 2017;18:966. doi: 10.3390/ijms18050966.
    1. Cheng F., Yan D., Chen J., Keidar M., Sotomayor E. Cold Plasma with Immunomodulatory Properties Has Significant Anti-Lymphoma Activities in Vitro and In Vivo. Blood. 2019;134:5307. doi: 10.1182/blood-2019-131065.

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅