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Current Drug Delivery

Editor-in-Chief

ISSN (Print): 1567-2018
ISSN (Online): 1875-5704

Review Article

Delivery Systems for Plasma-reactive Species and their Applications in the Field of Biomedicine

Author(s): Esmaeil Biazar*, Farzaneh Aavani, Reza Zeinali, Bahareh Kheilnezhad, Kiana Taheri and Zahra Yahyaei

Volume 21, Issue 11, 2024

Published on: 19 January, 2024

Page: [1497 - 1514] Pages: 18

DOI: 10.2174/0115672018268207231124014915

Price: $65

Open Access Journals Promotions 2
Abstract

Cold atmospheric plasma (CAP) is an ionized matter with potential applications in various medical fields, ranging from wound healing and disinfection to cancer treatment. CAP's clinical usefulness stems from its ability to act as an adjustable source of reactive oxygen and nitrogen species (RONS), which are known to function as pleiotropic signaling agents within cells. Plasma-activated species, such as RONS, have the potential to be consistently and precisely released by carriers, enabling their utilization in a wide array of biomedical applications. Furthermore, understanding the behavior of CAP in different environments, including water, salt solutions, culture medium, hydrogels, and nanoparticles, may lead to new opportunities for maximizing its therapeutic potential. This review article sought to provide a comprehensive and critical analysis of current biomaterial approaches for the targeted delivery of plasma-activated species in the hope to boost therapeutic response and clinical applicability.

Keywords: Cold atmosphere plasma, RONS, control release, delivery, plasma treatment, electrons.

Graphical Abstract
[1]
Mott-Smith, H.M. History of “Plasmas”. Nature, 1971, 233(5316), 219-219.
[http://dx.doi.org/10.1038/233219a0] [PMID: 16063290]
[2]
Bittencourt, J.A. Fundamentals of plasma physics; Springer, 2004.
[http://dx.doi.org/10.1007/978-1-4757-4030-1]
[3]
Adhikari, B.; Khanal, R.J.H.P. Introduction to the plasma state of matter. Himalayan Phys., 2013, 4, 60.
[http://dx.doi.org/10.3126/hj.v4i0.9430]
[4]
Ehlbeck, J.; Schnabel, U.; Polak, M.; Winter, J.; von Woedtke, T.; Brandenburg, R.; von dem Hagen, T.; Weltmann, K-D. Low temperature atmospheric pressure plasma sources for microbial decontamination. J. Phys. D Appl. Phys., 2011, 44(1), 013002.
[http://dx.doi.org/10.1088/0022-3727/44/1/013002]
[5]
Murphy, A.B.; Uhrlandt, D. Foundations of high-pressure thermal plasmas. Plasma Sources Sci. Technol., 2018, 27(6), 063001.
[http://dx.doi.org/10.1088/1361-6595/aabdce]
[6]
Park, G.Y.; Park, S.J.; Choi, M.Y.; Koo, I.G.; Byun, J.H.; Hong, J.W.; Sim, J.Y.; Collins, G.J.; Lee, J.K. Atmospheric-pressure plasma sources for biomedical applications. Plasma Sources Sci. Technol., 2012, 21(4), 043001.
[http://dx.doi.org/10.1088/0963-0252/21/4/043001]
[7]
Von Woedtke, T.; Schmidt, A.; Bekeschus, S.; Wende, K.; Weltmann, K.D. Plasma medicine: A field of applied redox biology. in vivo 2019, 33(4), 1011-1026.
[http://dx.doi.org/10.21873/invivo.11570] [PMID: 31280189]
[8]
Reiazi, R.; Akbari, M.E.; Norozi, A.; Etedadialiabadi, M. Application of cold atmospheric plasma (CAP) in cancer therapy: A review. Int. J. Cancer Manag., 2017, 10(3)
[http://dx.doi.org/10.5812/ijcp.8728]
[9]
Yan, D.; Lin, L.; Zvansky, M.; Kohanzadeh, L.; Taban, S.; Chriqui, S.; Keidar, M. Improving seed germination by cold atmospheric plasma. Plasma, 2022, 5(1), 98-110.
[http://dx.doi.org/10.3390/plasma5010008]
[10]
Guo, L.; Xu, R.; Gou, L.; Liu, Z.; Zhao, Y.; Liu, D.; Zhang, L.; Chen, H.; Kong, M.G. Mechanism of virus inactivation by cold atmospheric-pressure plasma and plasma-activated water. Appl. Environ. Microbiol., 2018, 84(17), e00726-e18.
[http://dx.doi.org/10.1128/AEM.00726-18] [PMID: 29915117]
[11]
Chen, Z.; Garcia, G., Jr; Arumugaswami, V.; Wirz, R.E. Cold atmospheric plasma for SARS-CoV-2 inactivation. Phys. Fluids, 2020, 32(11), 111702.
[http://dx.doi.org/10.1063/5.0031332] [PMID: 33244211]
[12]
Nomura, Y. Investigation of blood coagulation effect of nonthermal multigas plasma jet in vitro and in vivo. J. Surg. Res., 2017, 219, 302-309.
[13]
Haertel, B.; Woedtke, T.; Weltmann, K.D.; Lindequist, U. Non-thermal atmospheric-pressure plasma possible application in wound healing. Biomol. Ther., 2014, 22(6), 477-490.
[http://dx.doi.org/10.4062/biomolther.2014.105] [PMID: 25489414]
[14]
Lee, J.H.; Jeong, W.S.; Seo, S.J.; Kim, H.W.; Kim, K.N.; Choi, E.H.; Kim, K.M. Non-thermal atmospheric pressure plasma functionalized dental implant for enhancement of bacterial resistance and osseointegration. Dent. Mater., 2017, 33(3), 257-270.
[http://dx.doi.org/10.1016/j.dental.2016.11.011] [PMID: 28088458]
[15]
Duske, K.; Jablonowski, L.; Koban, I.; Matthes, R.; Holtfreter, B.; Sckell, A.; Nebe, J.B.; von Woedtke, T.; Weltmann, K.D.; Kocher, T. Cold atmospheric plasma in combination with mechanical treatment improves osteoblast growth on biofilm covered titanium discs. Biomaterials, 2015, 52, 327-334.
[http://dx.doi.org/10.1016/j.biomaterials.2015.02.035] [PMID: 25818439]
[16]
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(1), 13754.
[http://dx.doi.org/10.1038/s41598-018-32077-y] [PMID: 30213992]
[17]
Eisenhauer, P.; Chernets, N.; Song, Y.; Dobrynin, D.; Pleshko, N.; Steinbeck, M.J.; Freeman, T.A. Chemical modification of extracellular matrix by cold atmospheric plasma-generated reactive species affects chondrogenesis and bone formation. J. Tissue Eng. Regen. Med., 2016, 10(9), 772-782.
[http://dx.doi.org/10.1002/term.2224] [PMID: 27510797]
[18]
Tan, F.; Fang, Y.; Zhu, L.; Al-Rubeai, M. Controlling stem cell fate using cold atmospheric plasma. Stem Cell Res. Ther., 2020, 11(1), 368.
[http://dx.doi.org/10.1186/s13287-020-01886-2] [PMID: 32847625]
[19]
Keidar, M. Plasma for cancer treatment. Plasma Sources Sci. Technol., 2015, 24(3), 033001.
[http://dx.doi.org/10.1088/0963-0252/24/3/033001]
[20]
Schlegel, J. Köritzer, J.; Boxhammer, V. Plasma in cancer treatment. Clin. Plasma Med., 2013, 1(2), 2-7.
[http://dx.doi.org/10.1016/j.cpme.2013.08.001]
[21]
Dubuc, A.; Monsarrat, P.; Virard, F.; Merbahi, N.; Sarrette, J.P.; Laurencin-Dalicieux, S.; Cousty, S. Use of cold-atmospheric plasma in oncology: A concise systematic review. Ther. Adv. Med. Oncol., 2018, 10, 1758835918786475.
[http://dx.doi.org/10.1177/1758835918786475] [PMID: 30046358]
[22]
Izadjoo, M. Medical applications of cold atmospheric plasma: State of the science. J. Wound Care, 2018, 27(S9), S4-S10.
[http://dx.doi.org/10.12968/jowc.2018.27.Sup9.S4]
[23]
Borges, A.C.; Lima, G.M.G.; Nishime, T.M.C.; Gontijo, A.V.L.; Kostov, K.G.; Koga-Ito, C.Y. Amplitude-modulated cold atmospheric pressure plasma jet for treatment of oral candidiasis: In vivo study. PLoS One, 2018, 13(6), e0199832.
[http://dx.doi.org/10.1371/journal.pone.0199832] [PMID: 29949638]
[24]
Bernhardt, T. Plasma medicine: Applications of cold atmospheric pressure plasma in dermatology. Oxid. Med. Cell. Longev., 2019, 2019, 3873928.
[http://dx.doi.org/10.1155/2019/3873928]
[25]
Laroussi, M. Plasma medicine: A brief introduction. Plasma, 2018, 1(1), 47-60.
[http://dx.doi.org/10.3390/plasma1010005]
[26]
Kong, M.G.; Keidar, M.; Ostrikov, K. Plasmas meet nanoparticles—where synergies can advance the frontier of medicine. J. Phys. D Appl. Phys., 2011, 44(17), 174018.
[http://dx.doi.org/10.1088/0022-3727/44/17/174018]
[27]
Tornin, J.; Labay, C.; Tampieri, F.; Ginebra, M.P.; Canal, C. Evaluation of the effects of cold atmospheric plasma and plasma-treated liquids in cancer cell cultures. Nat. Protoc., 2021, 16(6), 2826-2850.
[http://dx.doi.org/10.1038/s41596-021-00521-5] [PMID: 33990800]
[28]
Bekeschus, S.; Liebelt, G.; Menz, J.; Berner, J.; Sagwal, S.K.; Wende, K.; Weltmann, K.D.; Boeckmann, L.; von Woedtke, T.; Metelmann, H.R.; Emmert, S.; Schmidt, A. Tumor cell metabolism correlates with resistance to gas plasma treatment: The evaluation of three dogmas. Free Radic. Biol. Med., 2021, 167, 12-28.
[http://dx.doi.org/10.1016/j.freeradbiomed.2021.02.035] [PMID: 33711420]
[29]
Bruggeman, P.J.; Kushner, M.J.; Locke, B.R.; Gardeniers, J.G.E.; Graham, W.G.; Graves, D.B.; Hofman-Caris, R.C.H.M.; Maric, D.; Reid, J.P.; Ceriani, E.; Fernandez Rivas, D.; Foster, J.E.; Garrick, S.C.; Gorbanev, Y.; Hamaguchi, S.; Iza, F.; Jablonowski, H.; Klimova, E.; Kolb, J.; Krcma, F.; Lukes, P.; Machala, Z.; Marinov, I.; Mariotti, D.; Mededovic Thagard, S.; Minakata, D.; Neyts, E.C.; Pawlat, J.; Petrovic, Z.L.; Pflieger, R.; Reuter, S.; Schram, D.C. Schrِter, S.; Shiraiwa, M.; Tarabovل, B.; Tsai, P.A.; Verlet, J.R.R.; von Woedtke, T.; Wilson, K.R.; Yasui, K.; Zvereva, G. Plasma–liquid interactions: A review and roadmap. Plasma Sources Sci. Technol., 2016, 25(5), 053002.
[http://dx.doi.org/10.1088/0963-0252/25/5/053002]
[30]
Hsu, W.H.; Masim, F.C.P.; Porta, M.; Nguyen, M.T.; Yonezawa, T.; Balčytis, A.; Wang, X.; Rosa, L.; Juodkazis, S.; Hatanaka, K. Femtosecond laser-induced hard X-ray generation in air from a solution flow of Au nano-sphere suspension using an automatic positioning system. Opt. Express, 2016, 24(18), 19994-20001.
[http://dx.doi.org/10.1364/OE.24.019994] [PMID: 27607607]
[31]
Canal, C. Important parameters in plasma jets for the production of RONS in liquids for plasma medicine: A brief review. Front. Chem. Sci. Eng., 2019.
[32]
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. J. Clin. Biochem. Nutr., 2017, 60(1), 33-38.
[http://dx.doi.org/10.3164/jcbn.16-65] [PMID: 28163380]
[33]
Keidar, M.; Shashurin, A.; Volotskova, O.; Ann Stepp, M.; Srinivasan, P.; Sandler, A.; Trink, B. Cold atmospheric plasma in cancer therapy. Phys. Plasmas, 2013, 20(5), 057101.
[http://dx.doi.org/10.1063/1.4801516]
[34]
Adamovich, I.; Baalrud, S.D.; Bogaerts, A.; Bruggeman, P.J.; Cappelli, M.; Colombo, V.; Czarnetzki, U.; Ebert, U.; Eden, J.G.; Favia, P.; Graves, D.B.; Hamaguchi, S.; Hieftje, G.; Hori, M.; Kaganovich, I.D.; Kortshagen, U.; Kushner, M.J.; Mason, N.J.; Mazouffre, S.; Thagard, S.M.; Metelmann, H-R.; Mizuno, A.; Moreau, E.; Murphy, A.B.; Niemira, B.A.; Oehrlein, G.S.; Petrovic, Z.L.; Pitchford, L.C.; Pu, Y-K.; Rauf, S.; Sakai, O.; Samukawa, S.; Starikovskaia, S.; Tennyson, J.; Terashima, K.; Turner, M.M.; van de Sanden, M.C.M.; Vardelle, A. The 2017 Plasma Roadmap: Low temperature plasma science and technology. J. Phys. D Appl. Phys., 2017, 50(32), 323001.
[http://dx.doi.org/10.1088/1361-6463/aa76f5]
[35]
Harley, J.C.; Suchowerska, N.; McKenzie, D.R. Cancer treatment with gas plasma and with gas plasma–activated liquid: Positives, potentials and problems of clinical translation. Biophys. Rev., 2020, 12(4), 989-1006.
[http://dx.doi.org/10.1007/s12551-020-00743-z] [PMID: 32757133]
[36]
Kim, S.; Kim, C.H. Applications of plasma-activated liquid in the medical field. Biomedicines, 2021, 9(11), 1700.
[http://dx.doi.org/10.3390/biomedicines9111700] [PMID: 34829929]
[37]
Mohades, S.; Laroussi, M.; Sears, J.; Barekzi, N.; Razavi, H. Evaluation of the effects of a plasma activated medium on cancer cells. Phys. Plasmas, 2015, 22(12), 122001.
[http://dx.doi.org/10.1063/1.4933367]
[38]
Mateu-Sanz, M.; Ginebra, M.P. Tornín, J.; Canal, C. Cold atmospheric plasma enhances doxorubicin selectivity in metastasic bone cancer. Free Radic. Biol. Med., 2022, 189, 32-41.
[http://dx.doi.org/10.1016/j.freeradbiomed.2022.07.007] [PMID: 35843475]
[39]
Brunner, T.F.; Probst, F.A.; Troeltzsch, M.; Schwenk-Zieger, S.; Zimmermann, J.L.; Morfill, G.; Becker, S.; Harréus, U.; Welz, C. Primary cold atmospheric plasma combined with low dose cisplatin as a possible adjuvant combination therapy for HNSCC cells-an in-vitro study. Head Face Med., 2022, 18(1), 21.
[http://dx.doi.org/10.1186/s13005-022-00322-5] [PMID: 35768853]
[40]
Lee, C.M.; Jeong, Y.I.L.; Kook, M.S.; Kim, B.H. Combinatorial effect of cold atmosphere plasma (Cap) and the anticancer drug cisplatin on oral squamous cell cancer therapy. Int. J. Mol. Sci., 2020, 21(20), 7646.
[http://dx.doi.org/10.3390/ijms21207646] [PMID: 33076565]
[41]
Li, Y.; Tang, T.; Lee, H.J.; Song, K. Selective anti-cancer effects of plasma-activated medium and its high efficacy with cisplatin on hepatocellular carcinoma with cancer stem cell characteristics. Int. J. Mol. Sci., 2021, 22(8), 3956.
[http://dx.doi.org/10.3390/ijms22083956] [PMID: 33921230]
[42]
Kim, S.Y.; Kim, H.J.; Kang, S.U.; Kim, Y.E.; Park, J.K.; Shin, Y.S.; Kim, Y.S.; Lee, K.; Kim, C.H. Non-thermal plasma induces AKT degradation through turn-on the MUL1 E3 ligase in head and neck cancer. Oncotarget, 2015, 6(32), 33382-33396.
[http://dx.doi.org/10.18632/oncotarget.5407] [PMID: 26450902]
[43]
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), 6085.
[http://dx.doi.org/10.1038/s41598-017-05620-6] [PMID: 28729634]
[44]
Liao, X.; Su, Y.; Liu, D.; Chen, S.; Hu, Y.; Ye, X.; Wang, J.; Ding, T. Application of atmospheric cold plasma-activated water (PAW) ice for preservation of shrimps (Metapenaeus ensis). Food Control, 2018, 94, 307-314.
[http://dx.doi.org/10.1016/j.foodcont.2018.07.026]
[45]
Zhou, R.; Zhou, R.; Wang, P.; Xian, Y.; Mai-Prochnow, A.; Lu, X.; Cullen, P.J.; Ostrikov, K.K.; Bazaka, K. Plasma-activated water: Generation, origin of reactive species and biological applications. J. Phys. D Appl. Phys., 2020, 53(30), 303001.
[http://dx.doi.org/10.1088/1361-6463/ab81cf]
[46]
Shen, J.; Tian, Y.; Li, Y.; Ma, R.; Zhang, Q.; Zhang, J.; Fang, J. Bactericidal effects against S. aureus and physicochemical properties of plasma activated water stored at different temperatures. Sci. Rep., 2016, 6(1), 28505.
[http://dx.doi.org/10.1038/srep28505] [PMID: 27346695]
[47]
Bălan, G.G.; Roșca, I.; Ursu, E.L.; Doroftei, F.; Bostănaru, A.C.; Hnatiuc, E.; Năstasă, V.; Șandru, V.; Ștefănescu, G.; Trifan, A.; Mareș, M. Plasma-activated water: A new and effective alternative for duodenoscope reprocessing. Infect. Drug Resist., 2018, 11, 727-733.
[http://dx.doi.org/10.2147/IDR.S159243] [PMID: 29844690]
[48]
Joshi, S.G.; Cooper, M.; Yost, A.; Paff, M.; Ercan, U.K.; Fridman, G.; Friedman, G.; Fridman, A.; Brooks, A.D. Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrob. Agents Chemother., 2011, 55(3), 1053-1062.
[http://dx.doi.org/10.1128/AAC.01002-10] [PMID: 21199923]
[49]
Xu, X.; Muller, J.G.; Ye, Y.; Burrows, C.J. DNA-protein cross-links between guanine and lysine depend on the mechanism of oxidation for formation of C5 vs C8 guanosine adducts. J. Am. Chem. Soc., 2008, 130(2), 703-709.
[http://dx.doi.org/10.1021/ja077102a] [PMID: 18081286]
[50]
Lunov, O. Plasma will…. Br. J. Dermatol., 2016, 174(3), 486-487.
[http://dx.doi.org/10.1111/bjd.14428] [PMID: 27002574]
[51]
Liu, T.; Wu, L.; Babu, J.P.; Hottel, T.L.; Garcia-Godoy, F.; Hong, L. Effects of atmospheric non-thermal argon/oxygen plasma on biofilm viability and hydrophobicity of oral bacteria. Am. J. Dent., 2017, 30(1), 52-56.
[PMID: 29178715]
[52]
Li, Y.; Pan, J.; Ye, G.; Zhang, Q.; Wang, J.; Zhang, J.; Fang, J. In vitro studies of the antimicrobial effect of non‐thermal plasma‐activated water as a novel mouthwash. Eur. J. Oral Sci., 2017, 125(6), 463-470.
[http://dx.doi.org/10.1111/eos.12374] [PMID: 29024061]
[53]
Chen, Z. Cold atmospheric plasma activated deionized water using helium, argon, and nitrogen as feeding gas for cancer therapy. arxiv, 2022, 2022, 06121.
[54]
Su, X.; Tian, Y.; Zhou, H.; Li, Y.; Zhang, Z.; Jiang, B.; Yang, B.; Zhang, J.; Fang, J. Inactivation efficacy of nonthermal plasma-activated solutions against Newcastle disease virus. Appl. Environ. Microbiol., 2018, 84(9), e02836-e17.
[http://dx.doi.org/10.1128/AEM.02836-17] [PMID: 29475861]
[55]
Liu, Z.C.; Guo, L.; Liu, D.X.; Rong, M.Z.; Chen, H.L.; Kong, M.G. Chemical kinetics and reactive species in normal saline activated by a surface air discharge. Plasma Process. Polym., 2017, 14(4-5), 1600113.
[http://dx.doi.org/10.1002/ppap.201600113]
[56]
Chen, Z.; Lin, L.; Gjika, E.; Cheng, X.; Canady, J.; Keidar, M. Selective treatment of pancreatic cancer cells by plasma-activated saline solutions. IEEE Trans. Radiat. Plasma Med. Sci., 2018, 2(2), 116-120.
[http://dx.doi.org/10.1109/TRPMS.2017.2761192]
[57]
Jirásek, V.; Lukeš, P. Formation of reactive chlorine species in saline solution treated by non-equilibrium atmospheric pressure He/O 2 plasma jet. Plasma Sources Sci. Technol., 2019, 28(3), 035015.
[http://dx.doi.org/10.1088/1361-6595/ab0930]
[58]
Zhang, J.; Qu, K.; Zhang, X.; Wang, B.; Wang, W.; Bi, J.; Zhang, S.; Li, Z.; Kong, M.G.; Liu, D.; Liu, C. Discharge plasma-activated saline protects against abdominal sepsis by promoting bacterial clearance. Shock, 2019, 52(1), 92-101.
[http://dx.doi.org/10.1097/SHK.0000000000001232] [PMID: 30028781]
[59]
Lan, K.C.; Chao, S.C.; Wu, H.Y.; Chiang, C.L.; Wang, C.C.; Liu, S.H.; Weng, T.I. Salidroside ameliorates sepsis-induced acute lung injury and mortality via downregulating NF-κB and HMGB1 pathways through the upregulation of SIRT1. Sci. Rep., 2017, 7(1), 12026.
[http://dx.doi.org/10.1038/s41598-017-12285-8] [PMID: 28931916]
[60]
Sriskandan, S.; Altmann, D. The immunology of sepsis. J. Pathol.: A J. Pathol. Soci. Great Britain Ireland, 2008, 214(2), 211-223.
[http://dx.doi.org/10.1002/path.2274]
[61]
Kong, R.; Jia, G.; Cheng, Z.; Wang, Y.; Mu, M.; Wang, S.; Pan, S.; Gao, Y.; Jiang, H.; Dong, D.; Sun, B. Dihydroartemisinin enhances Apo2L/TRAIL-mediated apoptosis in pancreatic cancer cells via ROS-mediated up-regulation of death receptor 5. PLoS One, 2012, 7(5), e37222.
[http://dx.doi.org/10.1371/journal.pone.0037222] [PMID: 22666346]
[62]
Zhang, R.; Humphreys, I.; Sahu, R.P.; Shi, Y.; Srivastava, S.K. In vitro and in vivo induction of apoptosis by capsaicin in pancreatic cancer cells is mediated through ROS generation and mitochondrial death pathway. Apoptosis, 2008, 13(12), 1465-1478.
[http://dx.doi.org/10.1007/s10495-008-0278-6] [PMID: 19002586]
[63]
Freund, E.; Liedtke, K.R.; van der Linde, J.; Metelmann, H.R.; Heidecke, C.D.; Partecke, L.I.; Bekeschus, S. Physical plasma-treated saline promotes an immunogenic phenotype in CT26 colon cancer cells in vitro and in vivo. Sci. Rep., 2019, 9(1), 634.
[http://dx.doi.org/10.1038/s41598-018-37169-3] [PMID: 30679720]
[64]
Krysko, D.V.; Ravichandran, K.S.; Vandenabeele, P. Macrophages regulate the clearance of living cells by calreticulin. Nat. Commun., 2018, 9(1), 4644.
[http://dx.doi.org/10.1038/s41467-018-06807-9] [PMID: 30405101]
[65]
Yamazaki, T.; Hannani, D.; Poirier-Colame, V.; Ladoire, S.; Locher, C.; Sistigu, A.; Prada, N.; Adjemian, S.; Catani, J.P.; Freudenberg, M.; Galanos, C.; André, F.; Kroemer, G.; Zitvogel, L. Defective immunogenic cell death of HMGB1-deficient tumors: Compensatory therapy with TLR4 agonists. Cell Death Differ., 2014, 21(1), 69-78.
[http://dx.doi.org/10.1038/cdd.2013.72] [PMID: 23811849]
[66]
Tanaka, H.; Hosoi, Y.; Ishikawa, K.; Yoshitake, J.; Shibata, T.; Uchida, K.; Hashizume, H.; Mizuno, M.; Okazaki, Y.; Toyokuni, S.; Nakamura, K.; Kajiyama, H.; Kikkawa, F.; Hori, M. Low temperature plasma irradiation products of sodium lactate solution that induce cell death on U251SP glioblastoma cells were identified. Sci. Rep., 2021, 11(1), 18488.
[http://dx.doi.org/10.1038/s41598-021-98020-w] [PMID: 34531507]
[67]
Ishikawa, K.; Hosoi, Y.; Tanaka, H.; Jiang, L.; Toyokuni, S.; Nakamura, K.; Kajiyama, H.; Kikkawa, F.; Mizuno, M.; Hori, M. Non-thermal plasma–activated lactate solution kills U251SP glioblastoma cells in an innate reductive manner with altered metabolism. Arch. Biochem. Biophys., 2020, 688, 108414.
[http://dx.doi.org/10.1016/j.abb.2020.108414] [PMID: 32464090]
[68]
Liu, Y.; Nakatsu, Y.; Tanaka, H.; Koga, K.; Ishikawa, K.; Shiratani, M.; Hori, M. Effects of plasma-activated Ringer’s lactate solution on cancer cells: Evaluation of genotoxicity. Genes Environ., 2023, 45(1), 3.
[http://dx.doi.org/10.1186/s41021-023-00260-x] [PMID: 36639786]
[69]
Mateu-Sanz, M.; Tornín, J.; Brulin, B.; Khlyustova, A.; Ginebra, M.P.; Layrolle, P.; Canal, C. Cold plasma-treated ringer’s saline: A weapon to target osteosarcoma. Cancers, 2020, 12(1), 227.
[http://dx.doi.org/10.3390/cancers12010227] [PMID: 31963398]
[70]
Reyes-Carmona, J.F.; Felippe, M.S.; Felippe, W.T. A phosphate-buffered saline intracanal dressing improves the biomineralization ability of mineral trioxide aggregate apical plugs. J. Endod., 2010, 36(10), 1648-1652.
[http://dx.doi.org/10.1016/j.joen.2010.06.014] [PMID: 20850670]
[71]
Traylor, M.J.; Pavlovich, M.J.; Karim, S.; Hait, P.; Sakiyama, Y.; Clark, D.S.; Graves, D.B. Long-term antibacterial efficacy of air plasma-activated water. J. Phys. D Appl. Phys., 2011, 44(47), 472001.
[http://dx.doi.org/10.1088/0022-3727/44/47/472001]
[72]
Griseti, E.; Kolosnjaj-Tabi, J.; Gibot, L.; Fourquaux, I.; Rols, M.P.; Yousfi, M.; Merbahi, N.; Golzio, M. Pulsed electric field treatment enhances the cytotoxicity of plasma-activated liquids in a three-dimensional human colorectal cancer cell model. Sci. Rep., 2019, 9(1), 7583.
[http://dx.doi.org/10.1038/s41598-019-44087-5] [PMID: 31110227]
[73]
Yost, A.D.; Joshi, S.G. Atmospheric nonthermal plasma-treated PBS inactivates Escherichia coli by oxidative DNA damage. PLoS One, 2015, 10(10), e0139903.
[http://dx.doi.org/10.1371/journal.pone.0139903] [PMID: 26461113]
[74]
Yan, D.; Nourmohammadi, N.; Bian, K.; Murad, F.; Sherman, J.H.; Keidar, M. Stabilizing the cold plasma-stimulated medium by regulating medium’s composition. Sci. Rep., 2016, 6(1), 26016.
[http://dx.doi.org/10.1038/srep26016] [PMID: 27172875]
[75]
Shaw, P.; Kumar, N.; Privat-Maldonado, A.; Smits, E.; Bogaerts, A. Cold atmospheric plasma increases temozolomide sensitivity of three-dimensional glioblastoma spheroids via oxidative stress-mediated DNA damage. Cancers, 2021, 13(8), 1780.
[http://dx.doi.org/10.3390/cancers13081780] [PMID: 33917880]
[76]
Kaushik, N.K.; Ghimire, B.; Li, Y.; Adhikari, M.; Veerana, M.; Kaushik, N.; Jha, N.; Adhikari, B.; Lee, S.J.; Masur, K.; von Woedtke, T.; Weltmann, K.D.; Choi, E.H. Biological and medical applications of plasma-activated media, water and solutions. Biol. Chem., 2018, 400(1), 39-62.
[http://dx.doi.org/10.1515/hsz-2018-0226] [PMID: 30044757]
[77]
Duan, J.; Lu, X.; He, G. The selective effect of plasma activated medium in an in vitro co-culture of liver cancer and normal cells. J. Appl. Phys., 2017, 121(1), 013302.
[http://dx.doi.org/10.1063/1.4973484]
[78]
Mihai, C.T.; Mihaila, I.; Pasare, M.A.; Pintilie, R.M.; Ciorpac, M.; Topala, I. Cold atmospheric plasma-activated media improve paclitaxel efficacy on breast cancer cells in a combined treatment model. Curr. Issues Mol. Biol., 2022, 44(5), 1995-2014.
[http://dx.doi.org/10.3390/cimb44050135] [PMID: 35678664]
[79]
Li, Y.; Lv, Y.; Tang, M.; Choi, E.H.; Wang, J.; Lv, G.; Zhu, Y.; Wang, S.; Liu, Y. Low‐temperature plasma‐jet‐activated medium inhibited tumorigenesis of lung adenocarcinoma in a 3D in vitro culture model. Plasma Process. Polym., 2021, 18(11), 2100049.
[http://dx.doi.org/10.1002/ppap.202100049]
[80]
Yang, X.; Yang, C.; Wang, L.; Cao, Z.; Wang, Y.; Cheng, C.; Zhao, G.; Zhao, Y. Inhibition of basal cell carcinoma cells by cold atmospheric plasma activated solution and differential gene expression analysis. Int. J. Oncol., 2020, 56(5), 1262-1273.
[http://dx.doi.org/10.3892/ijo.2020.5009] [PMID: 32319578]
[81]
Jo, A.; Joh, H.M.; Bae, J.H.; Kim, S.J.; Chung, T.H.; Chung, J.W. Plasma activated medium prepared by a bipolar microsecond-pulsed atmospheric pressure plasma jet array induces mitochondria-mediated apoptosis in human cervical cancer cells. PLoS One, 2022, 17(8), e0272805.
[http://dx.doi.org/10.1371/journal.pone.0272805] [PMID: 35939492]
[82]
Jo, A.; Bae, J.H.; Yoon, Y.J.; Chung, T.H.; Lee, E.W.; Kim, Y.H.; Joh, H.M.; Chung, J.W. Plasma-activated medium induces ferroptosis by depleting FSP1 in human lung cancer cells. Cell Death Dis., 2022, 13(3), 212.
[http://dx.doi.org/10.1038/s41419-022-04660-9] [PMID: 35256587]
[83]
Sersenová, D. The effect of plasma activated medium and PBS on human melanoma cells compared with other cancer and normal cells. Preprints, 2021, 2021, 2021010068.
[http://dx.doi.org/10.20944/preprints202101.0068.v1]
[84]
Nguyen, M.K.; Lee, D.S. Injectable biodegradable hydrogels. Macromol. Biosci., 2010, 10(6), 563-579.
[http://dx.doi.org/10.1002/mabi.200900402] [PMID: 20196065]
[85]
Liu, Z.; Zheng, Y.; Dang, J.; Zhang, J.; Dong, F.; Wang, K.; Zhang, J. A novel antifungal plasma-activated hydrogel. ACS Appl. Mater. Interfaces, 2019, 11(26), 22941-22949.
[http://dx.doi.org/10.1021/acsami.9b04700] [PMID: 31184465]
[86]
Mørch, Ý.A.; Donati, I.; Strand, B.L.; Skjåk-Bræk, G. Effect of Ca2+, Ba2+, and Sr2+ on alginate microbeads. Biomacromolecules, 2006, 7(5), 1471-1480.
[http://dx.doi.org/10.1021/bm060010d] [PMID: 16677028]
[87]
Lee, K.Y.; Mooney, D.J. Alginate: Properties and biomedical applications. Prog. Polym. Sci., 2012, 37(1), 106-126.
[http://dx.doi.org/10.1016/j.progpolymsci.2011.06.003] [PMID: 22125349]
[88]
Labay, C.; Hamouda, I.; Tampieri, F.; Ginebra, M.P.; Canal, C. Production of reactive species in alginate hydrogels for cold atmospheric plasma-based therapies. Sci. Rep., 2019, 9(1), 16160.
[http://dx.doi.org/10.1038/s41598-019-52673-w] [PMID: 31695110]
[89]
Bello, A.B.; Kim, D.; Kim, D.; Park, H.; Lee, S.H. Engineering and functionalization of gelatin biomaterials: From cell culture to medical applications. Tissue Eng. Part B Rev., 2020, 26(2), 164-180.
[http://dx.doi.org/10.1089/ten.teb.2019.0256] [PMID: 31910095]
[90]
Echave, M.C.; Saenz del Burgo, L.; Pedraz, J.L.; Orive, G. Gelatin as biomaterial for tissue engineering. Curr. Pharm. Des., 2017, 23(24), 3567-3584.
[PMID: 28494717]
[91]
Labay, C. Roldán, M.; Tampieri, F.; Stancampiano, A.; Bocanegra, P.E.; Ginebra, M.P.; Canal, C. Enhanced generation of reactive species by cold plasma in gelatin solutions for selective cancer cell death. ACS Appl. Mater. Interfaces, 2020, 12(42), 47256-47269.
[http://dx.doi.org/10.1021/acsami.0c12930] [PMID: 33021783]
[92]
Hamouda, R.A. Synthesis and biological characterization of silver nanoparticles derived from the cyanobacterium Oscillatoria limnetica. Nature, 2019, 9(1), 1-17.
[http://dx.doi.org/10.1038/s41598-019-49444-y]
[93]
Solé‐Martí, X. Ceramic‐hydrogel composite as carrier for cold‐plasma reactive‐species: Safety and osteogenic capacity in vivo. Plasma Process. Polym., 2022, 2022, e2200155.
[94]
Bruggeman, P.; Leys, C. Non-thermal plasmas in and in contact with liquids. J. Phys. D Appl. Phys., 2009, 42(5), 053001.
[http://dx.doi.org/10.1088/0022-3727/42/5/053001]
[95]
Silva-Teixeira, R.; Laranjo, M.; Lopes, B.; Almeida-Ferreira, C.; Gonçalves, A.C.; Rodrigues, T.; Matafome, P.; Sarmento-Ribeiro, A.B.; Caramelo, F.; Botelho, M.F. Plasma activated media and direct exposition can selectively ablate retinoblastoma cells. Free Radic. Biol. Med., 2021, 171, 302-313.
[http://dx.doi.org/10.1016/j.freeradbiomed.2021.05.027] [PMID: 34022401]
[96]
Solé-Martí, X.; Vilella, T.; Labay, C.; Tampieri, F.; Ginebra, M.P.; Canal, C. Thermosensitive hydrogels to deliver reactive species generated by cold atmospheric plasma: A case study with methylcellulose. Biomater. Sci., 2022, 10(14), 3845-3855.
[http://dx.doi.org/10.1039/D2BM00308B] [PMID: 35678531]
[97]
Zhai, S. Successful treatment of vitiligo with cold atmospheric plasma‒activated hydrogel. J. Invest. Dermatol., 2021, 141(11), 2710-2719.
[http://dx.doi.org/10.1016/j.jid.2021.04.019]
[98]
Zhang, H.; Xu, S.; Zhang, J.; Wang, Z.; Liu, D.; Guo, L.; Cheng, C.; Cheng, Y.; Xu, D.; Kong, M.G.; Rong, M.; Chu, P.K. Plasma-activated thermosensitive biogel as an exogenous ROS carrier for post-surgical treatment of cancer. Biomaterials, 2021, 276, 121057.
[http://dx.doi.org/10.1016/j.biomaterials.2021.121057] [PMID: 34399120]
[99]
Rivet, C-A. Impaired signaling in senescing T cells: Investigation of the role of reactive oxygen species using microfluidic platforms and computational modeling; Georgia Institute of Technology, 2012.
[100]
Cano, I.; Selivanov, V.; Gomez-Cabrero, D.; Tegnér, J.; Roca, J.; Wagner, P.D.; Cascante, M. Oxygen pathway modeling estimates high reactive oxygen species production above the highest permanent human habitation. PLoS One, 2014, 9(11), e111068.
[http://dx.doi.org/10.1371/journal.pone.0111068] [PMID: 25375931]
[101]
Markevich, N.I.; Markevich, L.N.; Hoek, J.B. Computational modeling analysis of generation of reactive oxygen species by mitochondrial assembled and disintegrated complex II. Front. Physiol., 2020, 11, 557721.
[http://dx.doi.org/10.3389/fphys.2020.557721] [PMID: 33178032]
[102]
Chen, Q.; Lesnefsky, E.J. Time to target mitochondrial reactive oxygen species generation from complex I. Function, 2022, 3(2), zqac010.
[http://dx.doi.org/10.1093/function/zqac010] [PMID: 35359911]
[103]
Lu, X.; Keidar, M.; Laroussi, M.; Choi, E.; Szili, E.J.; Ostrikov, K. Transcutaneous plasma stress: From soft-matter models to living tissues. Mater. Sci. Eng. Rep., 2019, 138, 36-59.
[http://dx.doi.org/10.1016/j.mser.2019.04.002]
[104]
Thulliez, M.; Bastin, O.; Nonclercq, A.; Delchambre, A.; Reniers, F. Gel models to assess distribution and diffusion of reactive species from cold atmospheric plasma: An overview for plasma medicine applications. J. Phys. D Appl. Phys., 2021, 54(46), 463001.
[http://dx.doi.org/10.1088/1361-6463/ac1623]
[105]
Chupradit, S.; Widjaja, G.; Radhi Majeed, B.; Kuznetsova, M.; Ansari, M.J.; Suksatan, W.; Turki Jalil, A.; Ghazi Esfahani, B. Recent advances in cold atmospheric plasma (CAP) for breast cancer therapy. Cell Biol. Int., 2023, 47(2), 327-340.
[http://dx.doi.org/10.1002/cbin.11939] [PMID: 36342241]
[106]
Ni, J.; Cozzi, P.; Hao, J.; Duan, W.; Graham, P.; Kearsley, J.; Li, Y. Cancer stem cells in prostate cancer chemoresistance. Curr. Cancer Drug Targets, 2014, 14(3), 225-240.
[http://dx.doi.org/10.2174/1568009614666140328152459] [PMID: 24720286]
[107]
Dai, X.; Zhu, K. Cold atmospheric plasma: Novel opportunities for tumor microenvironment targeting. Cancer Med., 2023, 12(6), 7189-7206.
[http://dx.doi.org/10.1002/cam4.5491] [PMID: 36762766]
[108]
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(3), 367-377.
[http://dx.doi.org/10.1586/erd.13.4] [PMID: 23668708]
[109]
Aryal, S.; Bisht, G. New paradigm for a targeted cancer therapeutic approach: A short review on potential synergy of gold nanoparticles and cold atmospheric plasma. Biomedicines, 2017, 5(4), 38.
[http://dx.doi.org/10.3390/biomedicines5030038] [PMID: 28671579]
[110]
Privat-Maldonado, A. Ros from physical plasmas: Redox chemistry for biomedical therapy. Oxid. Med. Cell. Longev., 2019, 2019, 9062098.
[http://dx.doi.org/10.1155/2019/9062098]
[111]
Yan, D.; Sherman, J.H.; Keidar, M. Cold atmospheric plasma, a novel promising anti-cancer treatment modality. Oncotarget, 2017, 8(9), 15977-15995.
[http://dx.doi.org/10.18632/oncotarget.13304] [PMID: 27845910]
[112]
Živanić, M.; Espona-Noguera, A.; Lin, A.; Canal, C. Current state of cold atmospheric plasma and cancer‐immunity cycle: Therapeutic relevance and overcoming clinical limitations using hydrogels. Adv. Sci., 2023, 10(8), 2205803.
[http://dx.doi.org/10.1002/advs.202205803] [PMID: 36670068]
[113]
Abdollahimajd, F. Cold plasma as a potential adjunctive therapy in COVID-19: Report of three cases. Authorea Preprints, 2021, 2021, 98515273.
[http://dx.doi.org/10.22541/au.160864749.98515273/v3]

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