Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Non-Thermal Atmospheric-Pressure Plasma Possible Application in Wound Healing

  • Haertel, Beate (Department of Pharmaceutical Biology, Institute of Pharmacy, Ernst-Moritz-Arndt University of Greifswald) ;
  • von Woedtke, Thomas (Leibniz Institute of Plasma Science and Technology Greifswald e.V (INP)) ;
  • Weltmann, Klaus-Dieter (Leibniz Institute of Plasma Science and Technology Greifswald e.V (INP)) ;
  • Lindequist, Ulrike (Department of Pharmaceutical Biology, Institute of Pharmacy, Ernst-Moritz-Arndt University of Greifswald)
  • Received : 2014.09.24
  • Accepted : 2014.11.10
  • Published : 2014.11.30
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Abstract

Non-thermal atmospheric-pressure plasma, also named cold plasma, is defined as a partly ionized gas. Therefore, it cannot be equated with plasma from blood; it is not biological in nature. Non-thermal atmospheric-pressure plasma is a new innovative approach in medicine not only for the treatment of wounds, but with a wide-range of other applications, as e.g. topical treatment of other skin diseases with microbial involvement or treatment of cancer diseases. This review emphasizes plasma effects on wound healing. Non-thermal atmospheric-pressure plasma can support wound healing by its antiseptic effects, by stimulation of proliferation and migration of wound relating skin cells, by activation or inhibition of integrin receptors on the cell surface or by its pro-angiogenic effect. We summarize the effects of plasma on eukaryotic cells, especially on keratinocytes in terms of viability, proliferation, DNA, adhesion molecules and angiogenesis together with the role of reactive oxygen species and other components of plasma. The outcome of first clinical trials regarding wound healing is pointed out.

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References

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  69. Atomic scale understanding of the permeation of plasma species across native and oxidized membranes vol.51, pp.36, 2018, https://doi.org/10.1088/1361-6463/aad524
  70. Effects of the Pulse Polarity on Helium Plasma Jets: Discharge Characteristics, Key Reactive Species, and Inactivation of Myeloma Cell vol.38, pp.5, 2018, https://doi.org/10.1007/s11090-018-9920-4
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  73. Various DC-driven point-to-plain discharges as non-thermal plasma sources and their bactericidal effects vol.27, pp.6, 2018, https://doi.org/10.1088/1361-6595/aabdd0
  74. Characterization of novel pin-hole based plasma source for generation of discharge in liquids supplied by DC non-pulsing voltage vol.27, pp.6, 2018, https://doi.org/10.1088/1361-6595/aac521
  75. Non-thermal plasma treatment improves chicken sperm motility via the regulation of demethylation levels vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-26049-5
  76. Contribution to the Chemistry of Plasma-Activated Water vol.44, pp.1, 2018, https://doi.org/10.1134/S1063780X18010075
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  78. Coagulation, deformability, and aggregation of RBCs and platelets following exposure to dielectric barrier discharge plasma with the use of different feeding gases vol.52, pp.15, 2019, https://doi.org/10.1088/1361-6463/ab0198
  79. A measurement method for determining the correlation between the amount of haemolysis and the electric current in low-temperature plasma treatment pp.16128850, 2019, https://doi.org/10.1002/ppap.201800142
  80. Cold atmospheric plasma ameliorates imiquimod-induced psoriasiform dermatitis in mice by mediating antiproliferative effects pp.1029-2470, 2019, https://doi.org/10.1080/10715762.2018.1564920
  81. Promotion Effects of Ultra-High Molecular Weight Poly-γ-Glutamic Acid on Wound Healing vol.25, pp.6, 2014, https://doi.org/10.4014/jmb.1412.12083
  82. Treatment of oral hyperpigmentation and gummy smile using lasers and role of plasma as a novel treatment technique in dentistry: An introductory review vol.8, pp.12, 2014, https://doi.org/10.18632/oncotarget.14887
  83. Influence of non-thermal plasma on structural and electrical properties of globular and nanostructured conductive polymer polypyrrole in water suspension vol.7, pp.None, 2017, https://doi.org/10.1038/s41598-017-15184-0
  84. Benefits of applying low-temperature plasma treatment to wound care and hemostasis from the viewpoints of physics and pathology vol.50, pp.50, 2014, https://doi.org/10.1088/1361-6463/aa945e
  85. Laser absorption spectroscopy for measurement of He metastable atoms of a microhollow cathode plasma vol.57, pp.1, 2014, https://doi.org/10.7567/jjap.57.01aa03
  86. 비열 유전체장벽방전 플라즈마의 포도상구균 및 대장균 살균효과 vol.28, pp.1, 2014, https://doi.org/10.15269/jksoeh.2018.28.1.61
  87. Synergistic effects of plasma-activated medium and chemotherapeutic drugs in cancer treatment vol.51, pp.13, 2018, https://doi.org/10.1088/1361-6463/aaafc4
  88. Cold atmospheric plasma as a potential tool for multiple myeloma treatment vol.9, pp.26, 2018, https://doi.org/10.18632/oncotarget.24649
  89. The kINPen—a review on physics and chemistry of the atmospheric pressure plasma jet and its applications vol.51, pp.23, 2018, https://doi.org/10.1088/1361-6463/aab3ad
  90. Application of cold plasma for performing a typical resection of the spleen vol.4, pp.5, 2014, https://doi.org/10.1088/2057-1976/aadb2d
  91. Effect of cold atmospheric plasma (CAP) on human adenoviruses is adenovirus type-dependent vol.13, pp.10, 2014, https://doi.org/10.1371/journal.pone.0202352
  92. Plasma Farming: Non-Thermal Dielectric Barrier Discharge Plasma Technology for Improving the Growth of Soybean Sprouts and Chickens vol.1, pp.2, 2018, https://doi.org/10.3390/plasma1020025
  93. Plasma cupping induces VEGF expression in skin cells through nitric oxide-mediated activation of hypoxia inducible factor 1 vol.9, pp.None, 2014, https://doi.org/10.1038/s41598-019-40086-8
  94. Short exposure to cold atmospheric plasma induces senescence in human skin fibroblasts and adipose mesenchymal stromal cells vol.9, pp.None, 2014, https://doi.org/10.1038/s41598-019-45191-2
  95. Aspergillus oryzae spore germination is enhanced by non-thermal atmospheric pressure plasma vol.9, pp.None, 2014, https://doi.org/10.1038/s41598-019-47705-4
  96. Fluorescence measurements of peroxynitrite/peroxynitrous acid in cold air plasma treated aqueous solutions vol.21, pp.17, 2019, https://doi.org/10.1039/c9cp00871c
  97. High-voltage applications of the triboelectric nanogenerator-Opportunities brought by the unique energy technology vol.6, pp.None, 2019, https://doi.org/10.1557/mre.2020.2
  98. The future for plasma science and technology vol.16, pp.1, 2014, https://doi.org/10.1002/ppap.201800118
  99. Electron characterization in weakly ionized collisional plasmas: from principles to techniques vol.4, pp.1, 2019, https://doi.org/10.1080/23746149.2018.1526114
  100. Regulation of Redox Homeostasis by Nonthermal Biocompatible Plasma Discharge in Stem Cell Differentiation vol.2019, pp.None, 2019, https://doi.org/10.1155/2019/2318680
  101. Improved Wound Healing of Airway Epithelial Cells Is Mediated by Cold Atmospheric Plasma: A Time Course-Related Proteome Analysis vol.2019, pp.None, 2014, https://doi.org/10.1155/2019/7071536
  102. ROS from Physical Plasmas: Redox Chemistry for Biomedical Therapy vol.2019, pp.None, 2014, https://doi.org/10.1155/2019/9062098
  103. Spatially resolved laser absorption spectroscopy on a micro-hollow cathode He plasma vol.58, pp.1, 2019, https://doi.org/10.7567/1347-4065/aaec19
  104. Liquid dynamics in response to an impinging low-temperature plasma jet vol.52, pp.7, 2014, https://doi.org/10.1088/1361-6463/aaf460
  105. Plasma-sensitive Escherichia coli mutants reveal plasma resistance mechanisms vol.16, pp.152, 2014, https://doi.org/10.1098/rsif.2018.0846
  106. Development of continuous metal patterns using two-dimensional atmospheric-pressure plasma-jet: on application to fabricate electrode on a flexible surface for film touch sensor vol.29, pp.4, 2014, https://doi.org/10.1088/1361-6439/ab0705
  107. Investigation of the mechanism of enhanced and directed differentiation of neural stem cells by an atmospheric plasma jet: A gene-level study vol.125, pp.16, 2014, https://doi.org/10.1063/1.5060650
  108. Design and characteristics investigation of a miniature low-temperature plasma spark discharge device vol.21, pp.5, 2019, https://doi.org/10.1088/2058-6272/aaf111
  109. Progress and perspectives in dry processes for emerging multidisciplinary applications: how can we improve our use of dry processes? vol.58, pp.5, 2014, https://doi.org/10.7567/1347-4065/ab163a
  110. Effect of liquid-dissolved gas components on concentrations of the aqueous reactive oxygen and nitrogen species vol.125, pp.22, 2014, https://doi.org/10.1063/1.5085258
  111. Cold atmospheric plasma-induced acidification of tissue surface: visualization and quantification using agarose gel models vol.52, pp.24, 2014, https://doi.org/10.1088/1361-6463/ab1119
  112. The molecular chaperone Hsp33 is activated by atmospheric-pressure plasma protecting proteins from aggregation vol.16, pp.155, 2014, https://doi.org/10.1098/rsif.2018.0966
  113. Liquid-type non-thermal atmospheric plasma ameliorates vocal fold scarring by modulating vocal fold fibroblast vol.244, pp.10, 2014, https://doi.org/10.1177/1535370219850084
  114. Modulation of Metamorphic and Regenerative Events by Cold Atmospheric Pressure Plasma Exposure in Tadpoles, Xenopus laevis vol.9, pp.14, 2014, https://doi.org/10.3390/app9142860
  115. Sublethal treatment with plasma-activated medium induces senescence-like growth arrest of A549 cells: involvement of intracellular mobile zinc vol.65, pp.1, 2014, https://doi.org/10.3164/jcbn.19-17
  116. Plasma activated radix arnebiae oil as innovative antimicrobial and burn wound healing agent vol.52, pp.33, 2019, https://doi.org/10.1088/1361-6463/ab234c
  117. Regeneration and Repair of Skin Wounds: Various Strategies for Treatment vol.18, pp.3, 2014, https://doi.org/10.1177/1534734619859214
  118. Wound Healing Potential of Low Temperature Plasma in Human Primary Epidermal Keratinocytes vol.16, pp.6, 2019, https://doi.org/10.1007/s13770-019-00215-w
  119. Plasma skincare device based on floating electrode dielectric barrier discharge vol.21, pp.12, 2014, https://doi.org/10.1088/2058-6272/ab428a
  120. Delivery and quantification of hydrogen peroxide generated via cold atmospheric pressure plasma through biological material vol.52, pp.50, 2014, https://doi.org/10.1088/1361-6463/ab4539
  121. The Role of Thermal Effects in Plasma Medical Applications: Biological and Calorimetric Analysis vol.9, pp.24, 2014, https://doi.org/10.3390/app9245560
  122. Immediate intervention effect of dielectric barrier discharge on acute inflammation in rabbit’s ear wound vol.10, pp.2, 2014, https://doi.org/10.1063/1.5139953
  123. Evaluation of the bactericidal effect of cold atmospheric pressure plasma on contaminated human bone: an in vitro study vol.58, pp.3, 2020, https://doi.org/10.1016/j.bjoms.2020.01.003
  124. 1D fluid model of RF-excited cold atmospheric plasmas in helium with air gas impurities vol.27, pp.4, 2020, https://doi.org/10.1063/1.5145033
  125. Time-resolved characterization of a free plasma jet formed off the surface of a piezoelectric crystal vol.29, pp.4, 2014, https://doi.org/10.1088/1361-6595/ab7987
  126. A Dielectric Barrier Discharge Plasma Degrades Proteins to Peptides by Cleaving the Peptide Bond vol.40, pp.3, 2020, https://doi.org/10.1007/s11090-019-10053-2
  127. Effect of DC micro-plasma treatment on bacteria in its vegetative bacteria vol.863, pp.None, 2014, https://doi.org/10.1088/1757-899x/863/1/012031
  128. Effect of external axial magnetic field on a helium atmospheric pressure plasma jet and plasma-treated water vol.53, pp.21, 2020, https://doi.org/10.1088/1361-6463/ab78d6
  129. The efficacy and safety of cold atmospheric plasma as a novel therapy for diabetic wound in vitro and in vivo vol.17, pp.3, 2020, https://doi.org/10.1111/iwj.13341
  130. Anticancer Effects of Cold Atmospheric Plasma in Canine Osteosarcoma Cells vol.21, pp.12, 2020, https://doi.org/10.3390/ijms21124556
  131. Positive Effect of Cold Atmospheric Nitrogen Plasma on the Behavior of Mesenchymal Stem Cells Cultured on a Bone Scaffold Containing Iron Oxide-Loaded Silica Nanoparticles Catalyst vol.21, pp.13, 2014, https://doi.org/10.3390/ijms21134738
  132. Effect of Cold Atmospheric Plasma Therapy vs Standard Therapy Placebo on Wound Healing in Patients With Diabetic Foot Ulcers : A Randomized Clinical Trial vol.3, pp.7, 2020, https://doi.org/10.1001/jamanetworkopen.2020.10411
  133. Effects of Plasma-Activated Water on Skin Wound Healing in Mice vol.8, pp.7, 2014, https://doi.org/10.3390/microorganisms8071091
  134. Influence of Plasma-Activated Water on Physical and Physical-Chemical Soil Properties vol.12, pp.9, 2014, https://doi.org/10.3390/w12092357
  135. Non-thermal dielectric-barrier discharge plasma induces reactive oxygen species by epigenetically modifying the expression of NADPH oxidase family genes in keratinocytes vol.37, pp.None, 2014, https://doi.org/10.1016/j.redox.2020.101698
  136. The effect of non‐thermal atmospheric pressure plasma application on wound healing after gingivectomy vol.17, pp.5, 2020, https://doi.org/10.1111/iwj.13379
  137. The formation of atomic oxygen and hydrogen in atmospheric pressure plasmas containing humidity: picosecond two-photon absorption laser induced fluorescence and numerical simulations vol.29, pp.10, 2014, https://doi.org/10.1088/1361-6595/abab55
  138. Cold Plasma Treatment Accelerates Regeneration of the Skin after Mechanical Damage vol.54, pp.4, 2020, https://doi.org/10.1007/s10527-020-10019-1
  139. The Effect of Plasma Treatment on the Speed of Healing of Wounds Similar to battle wounds vol.928, pp.None, 2014, https://doi.org/10.1088/1757-899x/928/7/072103
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  141. Analysis of Hydroxyl Radical and Hydrogen Peroxide Generated in Helium-Based Atmospheric-Pressure Plasma Jet and in Different Solutions Treated by Plasma for Bioapplications vol.9, pp.11, 2014, https://doi.org/10.1149/2162-8777/ab9c78
  142. Thin Film Deposition by Atmospheric Pressure Dielectric Barrier Discharges Containing Eugenol: Discharge and Coating Characterizations vol.12, pp.11, 2020, https://doi.org/10.3390/polym12112692
  143. TRPA1 and TRPV1 channels participate in atmospheric-pressure plasma-induced [Ca 2+ ] i response vol.10, pp.None, 2014, https://doi.org/10.1038/s41598-020-66510-y
  144. Effects of Nonthermal Plasma on Morphology, Genetics and Physiology of Seeds: A Review vol.9, pp.12, 2014, https://doi.org/10.3390/plants9121736
  145. Wound treatment by low-temperature atmospheric plasmas and issues in plasma engineering for plasma medicine vol.59, pp.12, 2020, https://doi.org/10.35848/1347-4065/abc3a0
  146. Efficacy of Low-temperature Plasma for Treatment of Facial Rejuvenation in Asian Population vol.9, pp.9, 2021, https://doi.org/10.1097/gox.0000000000003812
  147. Cell cycle regulation in human hair follicle dermal papilla cells using nonthermal atmospheric pressure plasma-activated medium vol.100, pp.13, 2014, https://doi.org/10.1097/md.0000000000025409
  148. Molecular Mechanisms Underlying Cellular Responses to the Loading of Non-thermal Atmospheric Pressure Plasma-activated Solutions vol.141, pp.10, 2014, https://doi.org/10.1248/yakushi.21-00134
  149. Generation, Detection and Bio-protection of Reactive Oxygen Species/Free Radicals vol.141, pp.12, 2021, https://doi.org/10.1248/yakushi.21-00164
  150. Redox Enzymes of the Thioredoxin Family as Potential and Novel Markers in Pemphigus vol.2021, pp.None, 2014, https://doi.org/10.1155/2021/6672693
  151. Head and Neck Cancer Cell Death due to Mitochondrial Damage Induced by Reactive Oxygen Species from Nonthermal Plasma-Activated Media: Based on Transcriptomic Analysis vol.2021, pp.None, 2014, https://doi.org/10.1155/2021/9951712
  152. Transdermal delivery of topical lidocaine in a mouse model is enhanced by treatment with cold atmospheric plasma vol.20, pp.2, 2021, https://doi.org/10.1111/jocd.13581
  153. Analysing Mouse Skin Cell Behaviour under a Non-Thermal kHz Plasma Jet vol.11, pp.3, 2014, https://doi.org/10.3390/app11031266
  154. Molecular mechanisms of non-thermal atmospheric pressure plasma-induced cellular responses vol.60, pp.2, 2014, https://doi.org/10.35848/1347-4065/abd496
  155. Selective inhibition of melanoma and basal cell carcinoma cells by short-lived species, long-lived species, and electric fields generated from cold plasma vol.129, pp.16, 2014, https://doi.org/10.1063/5.0041218
  156. Fabrication of Photoactive Electrospun Cellulose Acetate Nanofibers for Antibacterial Applications vol.14, pp.9, 2014, https://doi.org/10.3390/en14092598
  157. The Effect of Non-Thermal Plasma on the Structural and Functional Characteristics of Human Spermatozoa vol.22, pp.9, 2014, https://doi.org/10.3390/ijms22094979
  158. Non-Thermal Atmospheric Pressure Argon-Sourced Plasma Flux Promotes Wound Healing of Burn Wounds and Burn Wounds with Infection in Mice through the Anti-Inflammatory Macrophages vol.11, pp.12, 2014, https://doi.org/10.3390/app11125343
  159. Inhibitory Effect of Cold Atmospheric Plasma on Chronic Wound-Related Multispecies Biofilms vol.11, pp.12, 2014, https://doi.org/10.3390/app11125441
  160. Cold Atmospheric Plasma Promotes the Immunoreactivity of Granulocytes In Vitro vol.11, pp.6, 2014, https://doi.org/10.3390/biom11060902
  161. Moving toward a Handheld “Plasma” Spectrometer for Elemental Analysis, Putting the Power of the Atom (Ion) in the Palm of Your Hand vol.26, pp.16, 2014, https://doi.org/10.3390/molecules26164761
  162. Cold Atmospheric Plasma (CAP) Technology and Applications vol.6, pp.2, 2014, https://doi.org/10.2200/s01107ed1v01y202105mec035
  163. Analgesic effect of topical lidocaine is enhanced by cold atmospheric plasma pretreatment in facial CO2 laser treatments vol.20, pp.9, 2014, https://doi.org/10.1111/jocd.13983
  164. Energy efficiency of voltage waveform tailoring for the generation of excited species in RF plasma jets operated in He/N2 mixtures vol.30, pp.9, 2021, https://doi.org/10.1088/1361-6595/ac1c4d
  165. Flow Spin-trapping ESR Detection of •OH and •H Radicals Derived from Helium Atmospheric-pressure Plasma at Gas-Liquid Interface Employing a Micro Open-flow Reactor vol.50, pp.9, 2014, https://doi.org/10.1246/cl.210282
  166. Plasma Bioscience and Medicines vol.30, pp.5, 2014, https://doi.org/10.5757/asct.2021.30.5.118
  167. Anti-Bacterial Action of Plasma Multi-Jets in the Context of Chronic Wound Healing vol.11, pp.20, 2014, https://doi.org/10.3390/app11209598
  168. Microplasma Treatment versus Negative Pressure Therapy for Promoting Wound Healing in Diabetic Mice vol.22, pp.19, 2014, https://doi.org/10.3390/ijms221910266
  169. The evaluation of efficacy of atmospheric pressure plasma in diabetic ulcers healing: A randomized clinical trial vol.34, pp.6, 2014, https://doi.org/10.1111/dth.15169
  170. The Anti-Fibrotic Effect of Cold Atmospheric Plasma on Localized Scleroderma In Vitro and In Vivo vol.9, pp.11, 2014, https://doi.org/10.3390/biomedicines9111545
  171. Non-thermal atmospheric pressure plasma as a powerful tool for the synthesis of rhenium-based nanostructures for the catalytic hydrogenation of 4-nitrophenol vol.11, pp.61, 2014, https://doi.org/10.1039/d1ra07416d
  172. Cold Atmospheric Plasma, Platelet-Rich Plasma, and Nitric Oxide Synthesis Inhibitor: Effects Investigation on an Experimental Model on Rats vol.12, pp.2, 2014, https://doi.org/10.3390/app12020590
  173. Improvement of Nanostructured Polythiophene Film Uniformity Using a Cruciform Electrode and Substrate Rotation in Atmospheric Pressure Plasma Polymerization vol.12, pp.1, 2022, https://doi.org/10.3390/nano12010032
  174. Cold helium plasma jet does not stimulate collagen remodeling in a 3D human dermal substitute vol.143, pp.None, 2014, https://doi.org/10.1016/j.bioelechem.2021.107985