Important parameters in plasma jets for the production of RONS in liquids for plasma medicine: A brief review

Abstract

Reactive oxygen and nitrogen species (RONS) are among the key factors in plasma medicine. They are generated by atmospheric plasmas in biological fluids, living tissues and in a variety of liquids. This ability of plasmas to create a delicate mix of RONS in liquids has been used to design remote or indirect treatments for oncological therapy by treating biological fluids by plasmas and putting them in contact with the tumour. Documented effects include selective cancer cell toxicity, even though the exact mechanisms involved are still under investigation. However, the “right” dose for suitable therapeutical activity is crucial and still under debate. The wide variety of plasma sources hampers comparisons. This review focuses on atmospheric pressure plasma jets as the most studied plasma devices in plasma medicine and compiles the conditions employed to generate RONS in relevant liquids and the concentration ranges obtained. The concentrations of H₂O₂, NO₂⁻, NO₃⁻ and short-lived oxygen species are compared critically to provide a useful overview for the reader.

Graphical abstract

Keywords

atmospheric plasma jets / liquids / ROS / RNS / plasma-dose

References

[1] Graves D B. Reactive species from cold atmospheric plasma: Implications for cancer therapy. Plasma Processes and Polymers, 2014, 11(12): 1120–1127

[2] Graves D B. Oxy-nitroso shielding burst model of cold atmospheric plasma therapeutics. Clinical Plasma Medicine, 2014, 2(2): 38–49

[3] Yan D, Sherman J H, Keidar M. Cold atmospheric plasma, a novel promising anti-cancer treatment modality. Oncotarget, 2017, 8(9): 15977–15995

[4] Weltmann K D, Von Woedtke T. Plasma medicine—current state of research and medical application. Plasma Physics and Controlled Fusion, 2017, 59(1): 014031

[5] Lu X, Laroussi M, Puech V. On atmospheric-pressure non-equilibrium plasma jets and plasma bullets. Plasma Sources Science & Technology, 2012, 21(3): 34005

[6] Iza F, Kim G J, Lee S M, Lee J K, Walsh J L, Zhang Y T, Kong M G. Microplasmas: Sources, particle kinetics, and biomedical applications. Plasma Processes and Polymers, 2008, 5(4): 322–344

[7] Reuter S, Von Woedtke T, Weltmann K D. The kINPen—a review on physics and chemistry of the atmospheric pressure plasma jet and its applications. Journal of Physics. D, Applied Physics, 2018, 51(23): 233001

[8] Golda J, Held J, Redeker B, Konkowski M, Beijer P, Sobota A, Kroesen G, Braithwaite N St J, Reuter S, Turner M M, Gans T, O’Connell D, Schulz-von der Gathen V. Concepts and characteristics of the “COST Reference Microplasma Jet”. Journal of Physics. D, Applied Physics, 2016, 49(8): 084003

[9] Kelly S, Golda J, Turner M M, Schulz-von der Gathen V. Gas and heat dynamics of a micro-scaled atmospheric pressure plasma reference jet. Journal of Physics. D, Applied Physics, 2015, 48(44): 444002

[10] Adamovich I, Baalrud S D, Bogaerts A, Bruggeman P J, Capelli M, Colombo V, Czarnetzki U, Ebert U, Eden J G, Favia P, The 2017 plasma roadmap: Low temperature plasma science and technology. Journal of Physics. D, Applied Physics, 2017, 50(32): 323001

[11] Kajiyama H, Utsumi F, Nakamura K, Tanaka H, Toyokuni S, Hori M, Kikkawa F. Future perspective of strategic non-thermal plasma therapy for cancer treatment. Journal of Clinical Biochemistry and Nutrition, 2016, 60(1): 33–38

[12] Keidar M, Shashurin A, Volotskova O, Stepp M A, Srinivasan P, Sandler A, Trink B. Cold atmospheric plasma in cancer therapy. Physics of Plasmas, 2013, 20(5): 057101

[13] Partecke L I, Evert K, Haugk J, Doering F, Normann L, Diedrich S, Weiss F U, Evert M, Huebner N O, Guenther C, et al. Tissue tolerable plasma (TTP) induces apoptosis in pancreatic cancer cells in vitro and in vivo. BMC Cancer, 2012, 12(1): 473–482

[14] Graves D B. The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. Journal of Physics. D, Applied Physics, 2012, 45(26): 263001

[15] Buxton G V, Greenstock C L, Helman W P, Ross A B. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (•OH/•O-) in aqueous solution. Journal of Physical and Chemical Reference Data, 1988, 17(2): 513–886

[16] Lukes P, Dolezalova E, Sisrova I, Clupek M. Aqueous-phase chemistry and bactericidal effects from an air discharge plasma in contact with water: Evidence for the formation of peroxynitrite through a pseudo-second-order post-discharge reaction of H₂O₂ and HNO₂. Plasma Sources Science & Technology, 2014, 23(1): 015019

[17] Bruggeman P J, Kushner M J, Locke B R, Gardeniers J G E, Graham W G, Graves D B, Hofman-Caris R C, Maric D, Reid J P, Ceriani E, et al. Plasma-liquid interactions: A review and roadmap. Plasma Sources Science & Technology, 2016, 25(5): 253002

[18] Kim Y H, Hong Y J, Baik K Y, Kwon G C, Choi J J, Cho G S, Uhm H S, Kim D Y, Choi E H. Measurement of reactive hydroxyl radical species inside the biosolutions during non-thermal atmospheric pressure plasma jet bombardment onto the solution. Plasma Chemistry and Plasma Processing, 2014, 34(3): 457–472

[19] Rumbach P, Bartels D M, Sankaran R M, Go D B. The solvation of electrons by an atmospheric-pressure plasma. Nature Communications, 2015, 6(1): 7248

[20] Bullock A T, Gavin D L, Ingram M D. Electron spin resonance detection of spin-trapped radicals formed during the glow-discharge electrolysis of aqueous solutions. Journal of the Chemical Society, Faraday Transactions I, 1980, 76(0): 648–653

[21] Tresp H, Hammer M U, Winter J, Weltmann K D, Reuter S. Quantitative detection of plasma-generated radicals in liquids by electron paramagnetic resonance spectroscopy. Journal of Physics. D, Applied Physics, 2013, 46(43): 435401

[22] Eisenberg G. Colorimetric determination of hydrogen peroxide. Industrial & Engineering Chemistry. Analytical Edition, 1943, 15(5): 327–328

[23] Oliveira M C, Pupo Nogueira R F, Gomes Neto J, Jardim W F, Rohwedder J J R. Flow injection spectrophotometric system for hydrogen peroxide monitoring in photo-Fenton degradation processes. Quimica Nova, 2001, 24(2): 188–190

[24] Griess P. Griess reagent: A solution of sulphanilic acid and a-naphthylamine in acetic acid which gives a pink colour on reaction with the solution obtained after decomposition of nitrosyl complexes. Chemische Berichte, 1897, 12: 427

[25] Ikeda J I, Tanaka H, Ishikawa K, Sakakita H, Ikehara Y, Hori M. Plasma-activated medium (PAM) kills human cancer-initiating cells. Pathology International, 2018, 68(1): 23–30

[26] Turrini E, Laurita R, Stancampiano A, Catanzaro E, Calcanbrini C, Maffei F, Gherardi M, Colombo V, Fimognari C. Cold atmospheric plasma induces apoptosis and oxidative stress pathway regulation in T-Lymphoblastoid leukemia cells. Oxidative Medicine and Cellular Longevity, 2017, 2017: 4271065

[27] Machala Z, Tarabova B, Sersenová D, Janda M, Hensel K. Plasma activated water chemical and antibacterial effects: Correlation with gaseous and aqueous reactive oxygen and nitrogen species, plasma sources and air flow conditions. Journal of Physics. D, Applied Physics, 2018, 52(3): 034002

[28] Girard P M, Arbabian A, Fleury M, Bauville G, Puech V, Dutreix M, Sousa J S. Synergistic effect of H₂O₂ and NO₂ in cell death induced by cold atmospheric He plasma. Scientific Reports, 2016, 6(1): 29098

[29] 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 (Basel), 2017, 9(6): 61

[30] Oh J S, Szili E J, Ito S, Hong S H, Gaur N, Furuta H, Short R D, Hatta A. Slow molecular transport of plasma-generated reactive oxygen and nitrogen species and O₂ through agarose as a surrogate for tissue. Plasma Medicine, 2015, 5(2-4): 125–143

[31] Girard F, Peret M, Dumont N, Badets V, Blanc S, Gazeli K, Noel C, Belmonte T, Marlin L, Cambus J P, Correlations between gaseous and liquid phase chemistries induced by cold atmospheric plasmas in a physiological buffer. Physical Chemistry Chemical Physics, 2018, 20(14): 9198–9210

[32] Gorbanev Y, O’Connell D, Chechik V. Non-thermal plasma in contact with water: The origin of species. Chemistry (Weinheim an der Bergstrasse, Germany), 2016, 22(10): 3496–3505

[33] Chauvin J, Judée F, Yousfi M, Vicendo P, Merbahi N. Analysis of reactive oxygen and nitrogen species generated in three liquid media by low temperature helium plasma jet. Scientific Reports, 2017, 7(1): 4562

[34] Yan D, Nourmohammadi N, Bian K, Murad F, Sherman J H, Keidar M. Stabilizing the cold plasma-stimulated medium by regulating medium’s composition. Scientific Reports, 2016, 6(1): 26016

[35] Mohades S, Laroussi M, Sears J, Barekzi N, Razavi H. Evaluation of the effects of a plasma activated medium on cancer cells. Physics of Plasmas, 2015, 22(12): 122001

[36] Canal C, Fontelo R, Hamouda I, Guillem-Marti J, Cvelbar U, Ginebra M P. Plasma-induced selectivity in bone cancer cells death. Free Radical Biology & Medicine, 2017, 110: 72–80

[37] Duan J, Lu X, He G. On the penetration depth of reactive oxygen and nitrogen species generated by a plasma jet through real biological tissue. Physics of Plasmas, 2017, 24(7): 073506

[38] Yang H, Lu R, Xian Y, Gan L, Lu X, Yang X. Effects of atmospheric pressure cold plasma on human hepatocarcinoma cell and its 5-fluorouracil resistant cell line. Physics of Plasmas, 2015, 22(12): 122006

[39] Takamatsu T, Kawate A, Uehara K, Oshita T, Miyahara H, Dobrynin D, Fridman G, Fridman A, Okino A. Bacterial inactivation in liquids using multi-gas plasmas. Plasma Medicine, 2012, 2(4): 237–247

[40] Kurake N, Tanaka H, Ishikawa K, Kondo T, Sekine M, Nakamura K, Kajiyama H, Kikkawa F, Mizuno M, Hori M. Cell survival of glioblastoma grown in medium containing hydrogen peroxide and/or nitrite, or in plasma-activated medium. Archives of Biochemistry and Biophysics, 2016, 605: 102–108

[41] 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. Scientific Reports, 2016, 6(1): 36282

[42] Attri P, Yusupov M, Park J H, Lingamdinne L P, Koduru J R, Shiratani M, Choi E H, Bogaerts A. Mechanism and comparison of needle-type non-thermal direct and indirect atmospheric pressure plasma jets on the degradation of dyes. Scientific Reports, 2016, 6(1): 34419

[43] Oh J, Szili E J, Ogawa K, Short R D, Ito M, Furuta H, Hatta A. UV–vis spectroscopy study of plasma-activated water: Dependence of the chemical composition on plasma exposure time and treatment distance. Japanese Journal of Applied Physics, 2017, 57(1): 0102B9

[44] Wende K, Williams P, Dalluge J, Van Gaens W, Aboubakr H, Bischof J, Voedtke T, Goyal S M, Weltmann K D, Bogaerts A, Identification of the biologically active liquid chemistry induced by a nonthermal atmospheric pressure plasma jet. Biointerphases, 2015, 10(2): 29518

[45] Bekeschus S, Kolata J, Winterbourn C, Kramer A, Turner R, Weltmann K D, Broker B, Masur K. Hydrogen peroxide: A central player in physical plasma-induced oxidative stress in human blood cells. Free Radical Research, 2014, 48(5): 542–549

[46] Winter J, Tresp H, Hammer M U, Iseni S, Kupsch S, Schmidt-Bleker A, Dunnbier M, Masur K, Weltmann K D, Reuter S. Tracking plasma generated H₂O₂ from gas into liquid phase and revealing its dominant impact on human skin cells. Journal of Physics. D, Applied Physics, 2014, 47(28): 285401

[47] Schmidt A, Dietrich S, Steuer A, Weltmann K D, Von Woedtke T, Masur K, Wende K. Non-thermal plasma activates human keratinocytes by stimulation of antioxidant and phase II pathways. Journal of Biological Chemistry, 2015, 290(11): 6731–6750

[48] Tresp H, Hammer M U, Weltmann K D, Reuter S. Effects of atmosphere composition and liquid type on plasma-generated reactive species in biologically relevant solutions. Plasma Medicine, 2013, 3(12): 45–55

[49] Van Boxem W, Van Der Paal J, Gorbanev Y, Vanuytsel S, Smits E, Dewilde S, Bogaerts A. Anti-cancer capacity of plasma-treated PBS: Effect of chemical composition on cancer cell cytotoxicity. Scientific Reports, 2017, 7(1): 16478

[50] Bekeschus S, Wende K, Hefny M M, Rödder K, Jablonowski H, Schmidt A, Von Woedtke T, Weltmann K D, Benedikt J. Oxygen atoms are critical in rendering THP-1 leukaemia cells susceptible to cold physical plasma-induced apoptosis. Scientific Reports, 2017, 7(1): 2791

[51] Anderson C E, Cha N R, Lindsay A D, Clark D S, Graves D B. The role of interfacial reactions in determining plasma–liquid chemistry. Plasma Chemistry and Plasma Processing, 2016, 36(6): 1393–1415

[52] Ito T, Uchida G, Nakajama A, Takenaka K, Setsuhara Y. Control of reactive oxygen and nitrogen species production in liquid by nonthermal plasma jet with controlled surrounding gas. Japanese Journal of Applied Physics, 2017, 56(1S): 01AC06

[53] Kim S J, Chung T H. Cold atmospheric plasma jet-generated RONS and their selective effects on normal and carcinoma cells. Scientific Reports, 2016, 6(1): 20332

[54] Girard F, Badets V, Blanc S, Gazeli K, Marlin L, Authier L, Svarnas P, Sojic N, Clement F, Arbault S. Formation of reactive nitrogen species including peroxynitrite in physiological buffer exposed to cold atmospheric plasma. Royal Society of Chemistry Advances, 2016, 6(82): 78457–78467

[55] Szili E J, Oh J S, Fukuhara H, Bhatia R, Gaur N, Nguyen C K, Hong S H, Ito S, Ogawa K, Kawada C, et al. Modelling the helium plasma jet delivery of reactive species into a 3D cancer tumour. Plasma Sources Science & Technology, 2018, 27(1): 14001

[56] Suzen S, Gurer-Orhan H, Saso L. Detection of reactive oxygen and nitrogen species by electron paramagnetic resonance (EPR) technique. Molecules (Basel, Switzerland), 2017, 22(1): 181

[57] 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. Royal Sosiety of Chemistry Advances, 2014, 4(75): 39901–39905

[58] Machala Z, Tarabova B, Hensel K, Spetlikova E, Sikurova L, Lukes P. Formation of ROS and RNS in water electro-sprayed through transient spark discharge in air and their bactericidal effects. Plasma Processes and Polymers, 2013, 10(7): 649–659

[59] Jablonowski H, Bussiahn R, Hammer M U, Weltmann K D, Von Woedtke T, Reuter S. Impact of plasma jet vacuum ultraviolet radiation on reactive oxygen species generation in bio-relevant liquids. Physics of Plasmas, 2015, 22(12): 122008

[60] Knake N, Reuter S, Niemi K, Schulz-Von Der Gathen V, Winter J. Absolute atomic oxygen density distributions in the effluent of a microscale atmospheric pressure plasma jet. Journal of Physics. D, Applied Physics, 2008, 41(19): 194006

[61] Gay-Mimbrera J, Garcia M C, Isla-Tejera B, Rodero-Serrano A, Garcia-Nieto A V, Ruano J. Clinical and biological principles of cold atmospheric plasma application in skin cancer. Advances in Therapy, 2016, 33(6): 894–909

[62] Ratovitski E A, Cheng X, Yan D, Sherman J H, Canady J, Trink B, Keidar M. Anti-cancer therapies of 21st century : Novel approach to treat human cancers using cold atmospheric plasma. Plasma Processes and Polymers, 2014, 11(12): 1128–1137

[63] Hensel K, Kučerová K, Tarabová B, Janda M, Machala Z, Sano K, Mihai C T, Ciorpac M, Gorgan L D, Jijie R, Pohoata V, Topala I. Effects of air transient spark discharge and helium plasma jet on water, bacteria, cells, and biomolecules. Biointerphases, 2015, 10(2): 029515

[64] Keidar M. A prospectus on innovations in the plasma treatment of cancer. Physics of Plasmas, 2018, 25(8): 083504

Acknowledgements

This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (Grant agreement No. 714793). Authors acknowledge the Ramon y Cajal fellowship of Cristina Canal. Support for the research of Maria Pau Ginebra was received through the “ICREA Academia” prize for excellence in research, funded by the Generalitat de Catalunya. Zdenko Machala acknowledges the support from Slovak Recearch and Development Agency grant APVV-17-0382.

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