Cold Atmospheric Plasma in Cancer Therapy: Molecular Insights, Novel Concepts, and Future Opportunities
DOI:
https://doi.org/10.48048/tis.2025.8753Keywords:
Cancer treatment, Clinical trials, Cold atmospheric plasma, Reactive oxygen and nitrogen speciesAbstract
Over the past 2 decades, cold atmospheric plasma (CAP) has been playing increasingly pivotal roles in cutting edge biomedical applications and has developed into an innovative field of research of growing importance. One promising new medical application of CAP is cancer treatment. Being able to richly induce both reactive oxygen and nitrogen species, CAP has been shown to effectively control events critical to cancer initiation/progression; selectively inducing Deoxyribonucleic acid (DNA) damage and apoptotic cell deaths, reducing tumor volume and vasculature, halting metastasis and conferring anti-tumor effects by taking advantage of e.g., synergies among and between chemotherapeutic drugs and nanoparticles. This paper discusses molecular and immunological mechanisms of CAP treatment as a potential tool against cancers, with a focus on the novel mechanisms by which CAP interacts with chemotherapeutic drugs and nanotechnology. We then attempt to draw parallels between what is already known about the mechanisms of CAP activity, some novel concepts and attempts of CAP synergy, and the knowledge we would need to develop CAP as a potential therapeutic strategy in oncotherapy.
HIGHLIGHTS
- This article focused on critical review of cold atmospheric plasma’s (CAP) application in cancer therapy.
- CAP technology in cancer treatment has been expected to cause a medical and therapeutic implications.
- CAP has strong anticancer efficacy and has been reported about the cell migration and apoptosis.
- The major role of reactive oxygen and nitrogen species of plasma discharge is to control the core state of cancer transition.
GRAPHICAL ABSTRACT
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C Hoffmann, C Berganza and J Zhang. Cold atmospheric plasma: Methods of production and application in dentistry and oncology. Medical Gas Research 2013, 3, 21.
A Fridman. Plasma chemistry. Cambridge University Press, Cambridge, 2008.
DB Graves. Reactive species from cold atmospheric plasma: Implications for cancer therapy. Plasma Processes and Polymers 2014, 11(12), 1120-1127.
J Schlegel, J Köritzer and V Boxhammer. Plasma in cancer treatment. Clinical Plasma Medicine 2013; 1(2), 2-7.
N Nandkumar. Plasma-the fourth state of matter. International Journal of Scientific & Technology Research 2014; 3(9), 49-52.
S Eliezer and Y Eliezer. The fourth state of matter: An introduction to plasma science. 2nd eds. IOP Publishing, Bristol and Philadelphia, 2001.
KTAL Burm. Plasma: The fourth state of matter. Plasma Chemistry and Plasma Processing 2012; 32(2), 401-407.
L Bárdos and H Baránková. Cold atmospheric plasma: Sources, processes, and applications. Thin Solid Films 2010; 518(23), 6705-6713.
G Isbary, T Shimizu, YF Li, W Stolz, HM Thomas, GE Morfill and JL Zimmermann. Cold atmospheric plasma devices for medical issues. Expert Review of Medical Devices 2013; 10(3), 367-377.
CV Suschek and C Opländer. The application of cold atmospheric plasma in medicine: The potential role of nitric oxide in plasma-induced effects. Clinical Plasma Medicine 2016; 4(1), 1-8.
S Emmert, F Brehmer, H Hänßle, A Helmke, N Mertens, R Ahmed, D Simon, D Wandke, W Maus-Friedrichs, G Däschlein, MP Schön and W Viöl. Atmospheric pressure plasma in dermatology: Ulcus treatment and much more. Clinical Plasma Medicine 2013; 1(1), 24-29.
M Izadjoo, S Zack, H Kim and J Skiba. Medical applications of cold atmospheric plasma: State of the science. Journal of Wound Care 2018; 27(9), S4-S10.
B Stratmann, TC Costea, C Nolte, J Hiller, J Schmidt, J Reindel, K Masur, W Motz, J Timm, W Kerner and D Tschoepe. Effect of cold atmospheric plasma therapy vs standard therapy placed on wound healing in patients with diabetic foot ulcers: A randomized clinical trial. JAMA Network Open 2020; 3(7), e2010411.
S Mirpour, S Fathollah, P Mansouri, B Larijani, M Ghoranneviss, MM Tehrani and MR Amini. Cold atmospheric plasma as an effective method to treat diabetic foot ulcers: A randomized clinical trial. Scientific Reports 2020; 10, 10440.
R He, Q Li, W Shen, T Wang, H Lu, J Lu, F Lu, M Luo, J Zhang, H Gao, D Wang, W Xing, W Jia and F Liu. The efficacy and safety of cold atmospheric plasma as a novel therapy for diabetic wound in vitro and in vivo. International Wound Journal 2020; 17, 851-863.
O Assadian, KJ Ousey, G Daeschlein, A Kramer, C Parker, J Tanner and DJ Leaper. Effects and safety of atmospheric low-temperature plasma on bacterial reduction in chronic wounds and wound size reduction: A systematic review and meta-analysis. International Wound Journal 2019; 16, 103-111.
F Brehmer, HA Haenssle, G Daeschlein, R Ahmed, S Pfeiffer, A Görlitz, D Simon, MP Schön, D Wandke and S Emmert. 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). Journal of the European Academy of Dermatology and Venereology 2015; 29, 148-155.
R Tiede, J Hirschberg, G Daeschlein, TV Woedtke, W Vioel and S Emmert. Plasma applications: A dermatological view. Contributions to Plasma Physics 2014; 54(2), 118-130.
J Heinlin, G Isbary, W Stolz, G Morfill, M Landthaler, T Shimizu, B Steffes, T Nosenko, JL Zimmermann and S Karrer. Plasma applications in medicine with a special focus on dermatology. Journal of the European Academy of Dermatology and Venereology 2011; 25(1), 1-11.
T Bernhardt, ML Semmler, M Schäfer, S Bekeschus, S Emmert and L Boeckmann. Plasma medicine: Applications of cold atmospheric pressure plasma in dermatology. Oxidative Medicine and Cellular Longevity 2019; 2019, 3873928.
R Ranjan, PV Krishnamraju, T Shankar and S Gowd. Nonthermal plasma in dentistry: An update. Journal of International Society of Preventive and Community Dentistry 2017; 7(3), 71-75.
V Arora, V Nikhil, NK Suri and P Arora. Cold atmospheric plasma (CAP) in dentistry. Dentistry 2014; 4, 1000189.
M Gherardi, R Tonini and V Colombo. Plasma in dentistry: Brief history and current status. Trends Biotechnology 2018; 36(6), 583-585.
S Hartwig, S Preissner, JO Voss, M Hertel, C Doll, R Waluga and JD Raguse. The feasibility of cold atmospheric plasma in the treatment of complicated wounds in cranio-maxillo-facial surgery. Journal of Cranio-Maxillofacial Surgery 2017; 45(10), 1724-1730.
M Pinelli, M Starnoni and GD Santis. The use of cold atmospheric plasma device in flap elevation. Plastic and Reconstructive Surgery - Global Open 2020; 8(5), e2815.
G Isbary, T Shimizu, JL Zimmermann, HM Thomas, GE Morfill and W Stolz. Cold atmospheric plasma for local infection control and subsequent pain reduction in a patient with chronic post-operative ear infection. New Microbes and New Infections 2013; 1(3), 41-43.
L Guo, R Xu, L Gou, Z Liu, Y Zhao, G Liu, L Zhang, H Chen and MG Kong. Mechanism of virus inactivation by cold atmospheric-pressure plasma and plasmaactivated water. Applied and Environmental Microbiology 2018; 84(17), e00726-18.
Z Chen, G Garcia, V Arumugaswami and RE Wirz. Cold atmospheric plasma for SARS-CoV-2 inactivation. Physics of Fluids 2020; 32, 111702.
A Filipić, I Gutierrez-Aguirre, G Primc, M Mozetič and G Dobnik. Cold plasma, a new hope in the field of virus inactivation. Trends Biotechnology 2020; 38(11), 1278-1291.
S Arndt, M Landthaler, JL Zimmermann, P Unger, E Wacker, T Shimizu, YF Li, GE Morfill, AK Bosserhoff and S Karrer. Effects of cold atmospheric plasma (CAP) on β-defensins, inflammatory cytokines, and apoptosis-related molecules in keratinocytes in vitro and in vivo. PLoS One 2015; 10(3), e0120041.
D Yan, Q Wang, A Malyavko, DB Zolotukhin, M Adhikari, JH Sherman and M Keidar. The anti-glioblastoma effect of cold atmospheric plasma treatment: Physical pathway v.s. chemical pathway. Scientific Reports 2020; 10, 11788.
D Yan, A Talbot, N Nourmohammadi, X Cheng, J Canady, J Sherman and M Keidar. Principles of using cold atmospheric plasma stimulated media for cancer treatment. Scientific Reports 2015; 5, 18339.
P Babington, K Rajjoub, J Canady, A Siu, M Keidar and JH Sherman. Use of cold atmospheric plasma in the treatment of cancer. Biointerphases 2015; 10(2), 029403.
C Welz, S Emmert, M Canis, S Becker, P Baumeister, T Shimizu, GE Morfill, U Harréus and JL Zimmermann. Cold atmospheric plasma: A promising complementary therapy for squamous head and neck cancer. PLoS One 2015; 10(11), e0141827.
HR Metelmann, DS Nedrelow, C Seebauer, M Schuster, TV Woedtke, KD Weltmann, S Kindler, PH Metelmann, SE Finkelstein, DDV Hoff and F podmelle. Head and neck cancer treatment and physical plasma. Clinical Plasma Medicine 2015; 3(1), 17-23.
X Zhou, D Cai, S Xiao, M Ning, R Zhou, S Zhang, X Chen, K Ostrikov and X Dai. InvivoPen: A novel plasma source for in vivo cancer treatment. Journal Cancer 2020; 11(8), 2273-2282.
M Keidar, R Walk, A Shashurin, P Srinivasan, A Sandler, S Dasgupta, R Ravi, R Guerrero-Preston and B Trink. Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. British Journal of Cancer 2011; 105, 1295-1301.
S Aryal and G Bisht. New paradigm for a targeted cancer therapeutic approach: A short review on potential synergy of gold nanoparticles and cold atmospheric plasma. Biomedicines 2017; 5(3), 38.
X Dai, K Bazaka, EW Thompson and KK Ostrikov. Cold atmospheric plasma: A promising controller of cancer cell states. Cancers 2020; 12(11), 3360.
O Volotskova, TS Hawley, MA Stepp and M Keidar. Targeting the cancer cell cycle by cold atmospheric plasma. Scientific Reports 2012; 2, 636.
S Arndt, E Wacker, YF Li, T Shimizu, HM Thomas, GE Morfill, S Karrer, JL Zimmermann and AK Bosserhoff. Cold atmospheric plasma, a new strategy to induce senescence in melanoma cells. Experimental Dermatology 2013; 22(4), 284-289.
J Xia, W Zeng, Y Xia, B Wang, D Xu, D Liu, MG Kong and Y Dong. Cold atmospheric plasma induces apoptosis of melanoma cells via Sestrin2-mediated nitric oxide synthase signaling. Journal of Biophotonics 2019; 12(1), e201800046.
DK Yadav, M Adhikari, S Kumar, B Ghimire, I Han, MH Kim and EH Choi. Cold atmospheric plasma generated reactive species aided inhibitory effects on human melanoma cells: An in vitro and in silico study. Scientific Reports 2020; 10, 3396.
G Pasqual-Melo, RK Gandhirajan, I Stoffels and S Bekeschus. Targeting malignant melanoma with physical plasmas. Clinical Plasma Medicine 2018; 10, 1-8.
HJ Ahn, K Kim, G Kim, E Moon, SS Yang and JS Lee. Atmospheric-pressure plasma jet induces apoptosis involving mitochondria via generation of free radicals. PLoS One 2011; 6(11), 28154.
X Yan, Z Xiong, F Zou, S Zhao, X Lu, G Yang, G He and K Ostrikov. Plasma-induced death of HepG2 cancer cells: Intracellular effects of reactive species. Plasma Processes and Polymers 2012; 9(1), 59-66.
M Adhikari, B Adhikari, A Adhikari, D Yan, V Soni, J Sherman and M Keidar. Cold atmospheric plasma as a novel therapeutic tool for the treatment of brain cancer. Current Pharmaceutical Design 2020; 26(19), 2195-2206.
A Privat-Maldonado, Y Gorbanev, S Dewilde, E Smits and A Bogaerts. Reduction of human glioblastoma spheroids using cold atmospheric plasma: The combined effect of short-and long-lived reactive species. Cancers 2018; 10(11), 394.
D Yan, H Cui, W Zhu, N Nourmohammadi, J Milberg, LG Zhang, JH Sherman and M Keidar. The specific vulnerabilities of cancer cells to the cold atmospheric plasma-stimulated solutions. Scientific Reports 2017; 7, 4479.
E Gjika, S Pal-Ghosh, ME Kirschner, I Lin, JH Sherman, MA Stepp and M Keidar. Combination therapy of cold atmospheric plasma (CAP) with temozolomide in the treatment of U87MG glioblastoma cells. Scientific Reports 2020; 10, 16495.
D Xu, N Ning, Y Xu, B Wang, Q Cui, Z Liu, X Wang, D Liu, H Chen and MG Kong. Effect of cold atmospheric plasma treatment on the metabolites of human leukemia cells. Cancer Cell International 2019; 19, 135.
F Cheng, D Yan, J Chen, M Keidar and E Sotomayor. Cold plasma with immunomodulatory properties has significant anti-lymphoma activities in vitro and in vivo. Blood 2019; 134(1), 5307.
D Xu, Y Xu, Q Cui, D Liu, Z Liu, X Wang, Y Yang, M Feng, R Liang, H Chen, K Ye and MG Kong. Cold atmospheric plasma as a potential tool for multiple myeloma treatment. Oncotarget 2018; 9(26), 18002-18017.
D Yan, JH Sherman and M Keidar. Cold atmospheric plasma, a novel promising anti-cancer treatment modality. Oncotarget 2017; 8(9), 15977-15995.
O Troitskaya, E Golubitskaya, M Biryukov, M Varlamov, P Gugin, E Milakhina, V Richter, I Schweigert, D Zakrevsky and O Koval. Non-thermal plasma application in tumor-bearing mice induces increase of serum HMGB1. International Journal of Molecular Sciences 2020; 21(14), 5128.
F Saadati, H Mahdikia, HA Abbaszadeh, MA Abdollahifar, MS Khoramgah and B Shokri. Comparison of direct and indirect cold atmospheric-pressure plasma methods in the B16F10 melanoma cancer cells treatment. Scientific Reports 2018; 8, 7689.
KR Liedtke, S Diedrich, O Pati, E Freund, R Flieger, CD Heidecke, LI Partecke and S Bekeschus. Cold physical plasma selectively elicits apoptosis in murine pancreatic cancer cells in vitro and in vivo. Anticancer Research 2018; 38(10), 5655-63.
MIE Gohary, FFE Aksher, SA Ghalab and MAA Ghazala. Effect of cold atmospheric plasma on ehrlich carcinoma. The Egyptian Journal of Biophysics and Biomedical Engineering 2016; 17, 29-39.
M Keidar, D Yan and JH Sherman. The anti-cancer effect of CAP treatment in vivo. In: Cold plasma cancer therapy. Morgan & Claypool Publishers, California, 2019, p. 5-12.
M Vandamme, E Robert, S Dozias, J Sobilo, S Lerondel, AL Pape and JM Pouvesle. Response of human glioma U87 xenografted on mice to non thermal plasma treatment. Plasma Medicine 2011; 1(1), 27-43.
N Georgescu and AR Lupu. Tumoral and normal cells treatment with high-voltage pulsed cold atmospheric plasma jets. IEEE Transactions on Plasma Science 2010; 38(8), 1949-55.
A Dubuc, P Monsarrat, F Virard, NMerbahi, JP Sarrette, S Laurencin-Dalicieux and S Cousty. Use of cold-atmospheric plasma in oncology: A concise systematic review. Therapeutic Advances in Medical Oncology 2018; 10, 1-12.
HB Baniya, S Panday, P Khadka, A Nepal, RP Guragain, GP Panta, S Dhungana, BG Shrestha and DP Subedi. Antimicrobial and anticancer efficacy of atmospheric pressure cold plasma technology. Materials International 2022; 4(1), 1.
HB Baniya, P Khadka, S Panday, A Nepal, RP Guragain, TR Lamichhane, S Dhungana, BG Shrestha and DP Subedi. Characterization of cold atmospheric pressure plasma technology and its anticancer properties. Plasma Medicine 2021; 11(4), 53-62.
NK Kaushik, B Ghimire, Y Li, M Adhikari, M Veerana, N Kaushik, N Jha, B Adhikari, SJ Lee, K Masur, TV Woedtke and KD Weltmann. Biological and medical applications of plasma-activated media, water and solutions. Biological Chemistry 2018; 400(1), 39-62.
M Adhikari, B Adhikari, B Ghimire, S Baboota and EH Choi. Cold atmospheric plasma and silymarin nano emulsion activate autophagy in human melanoma cells. International Journal of Molecular Sciences 2020; 21, 1939.
M Ishaq, MDM Evans and KK Ostrikov. 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. Biochimica Biohysica Acta 2014; 1834, 2827-37.
SU Kang, JH Cho, JW Chang, YS Shin, KI Kim, JK Park, SS Yang, JS Lee, E Moon, K Lee and CH Kim. Nonthermal plasma induces head and neck cancer cell death: The potential involvement of mitogen-activated protein kinase-dependent mitochondrial reactive oxygen species. Cell Death Disease 2014; 5, e1056.
M Ishaq, S Kumar, H Varinli, ZJ Han, AE Rider, MDM Evans, AB Murphy and K Ostrikov. Atmospheric gas plasma-induced ROS production activates TNF-ASK1 pathway for the induction of melanoma cancer cell apoptosis. Molecular Biology of the Cell 2014; 25(9), 1523-1531.
H Ichijo, E Nishida, K Irie, PT Dijke, M Saitoh, T Moriguchi, M Takagi, K Matsumoto, K Miyazono and Y Gotoh. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 1997; 275(5296), 90-94.
M Vandamme, E Robert, S Lerondel, V Sarron, D Ries, S Dozias, J Sobilo, D Gosset, C Kieda, B Legrain, JM Pouvesle and AL Pape. ROS implication in a new antitumor strategy based on non-thermal plasma. International Journal of Cancer 2012; 130(9), 2185-2194.
S Kalghatgi, CM Kelly, E Cerchar, B Torabi, O Alekseev, A Fridman, G Friedman and J Azizkhan-Clifford. Effects of non-thermal plasma on mammalian cells. PLoS One 2011; 6(1), e16270.
GJ Kim, W Kim, KT Kim and JK Lee. DNA damage and mitochondria dysfunction in cell apoptosis induced by nonthermal air plasma. Applied Physics Letters 2010; 96(2), 21502.
JW Chang, SU Kang, YS Shin, K Kiml, SJ Seo, SS Yang, JS Lee, E Moon, SJ Baek, K Lee and CH Kim. Non-thermal atmospheric pressure plasma induces apoptosis in oral cavity squamous cell carcinoma: Involvement of DNA-damage-triggering sub-G1 arrest via the ATM/p53 pathway. Archives of Biochemistry and Biophysics 2014; 545, 133-140.
S Burma, BP Chen, M Murphy, A Kurimasa and DJ Chen. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. Journal of Biological Chemistry 2001; 276(45), 42462-42467.
S Nowsheen and ES Yang. The intersection between DNA damage response and cell death pathways. Experimental Oncology 2012; 34, 243-254.
M Ishaq, K Bazaka and K Ostrikov. Intracellular effects of atmospheric-pressure plasmas on melanoma cancer cells. Physics of Plasmas 2015; 22(9), 122003.
HJ Lee, CH Shon, YS Kim, S Kim, GC Kim and MG Kong. Degradation of adhesion molecules of G361 melanoma cells by a non-thermal atmospheric pressure microplasma. New Journal of Physics 2009; 11, 115026.
A Shashurin, MA Stepp, TS Hawley, S Pal-Ghosh, L Brieda, S Bronnikov, A Jurjus and M Keidar. Influence of cold atmospheric plasma jet on surface integrin expression of living cells. Plasma Processes and Polymers 2010; 7(3-4), 294-300.
JW Chang, SU Kang, YS Shin, K Kim, SJ Seo, SS Yang, JS Lee, E Moon, K Lee and Ch Kim. Non-thermal atmospheric pressure plasma inhibits thyroid papillary cancer cell invasion via cytoskeletal modulation, altered MMP-2/-9/uPA activity. PLoS One 2014; 9(3), e92198.
TT Sein, AA Thant, Y Hiraiwa, ARMR Amin, Y Sohara, Y Liu, S Matsuda, T Yamamoto and M Hamaguchi. A role for FAK in the concanavalin A-dependent secretion of matrix metalloproteinase-2 and -9. Oncogene 2000; 19, 5539-5542.
A Lin, B Truong, A Pappas, L Kirifides, A Oubarri, S Chen, S Lin, D Dobrynin, G Fridman, A Fridman, N Sang and V Miller. Uniform nanosecond pulsed dielectric barrier discharge plasma enhances anti-tumor effects by induction of immunogenic cell death in tumors and stimulation of macrophages. Plasma Processes and Polymers 2015; 12(12), 1392-1399.
G Chen, Z Chen, D Wen, Z Wang, H Li, Y Zeng, G Dotti, RE Wirz and Z Gu. Transdermal cold atmospheric plasma-mediated immune checkpoint blockade therapy. Proceedings of the National Academy of Sciences 2020; 117(7), 3687-3692.
A Lin, Y Gorbanev, JD Backer, JV Loenhout, WV Boxem, F Lemière, P Cos, S Dewilde, E Smits and A Bogaerts. Non-thermal plasma as a unique delivery system of short-lived reactive oxygen and nitrogen species for immunogenic cell death in melanoma cells. Advanced Science 2019; 6(6), 1802062.
V Miller, A Lin and A Fridman. Why target immune cells for plasma treatment of cancer. Plasma Chemistry and Plasma Processing 2016; 36, 259-268.
G Kroemer, I Galluzzi, O Kepp and L Zitvogel. Immunogenic cell death in cancer therapy. Annual Review of Immunology 2013; 31, 51-72.
T Panaretakis, O Kepp, U Brockmeier, A Tesniere, AC Bjorklund, DC Chapman, M Durchschlag, N Joza, G Pierron, PV Endert, J Yuan, L Zitvogel, F Madeo, DB Williams and G Kroemer. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. The EMBO Journal 2009; 28, 578-590.
M Obeid, A Tesniere, F Ghiringhelli, GM Fimia, L Apetoh, JL Perfettini, M Castedo, G Mignot, T Panaretakis, N Casares, D Métivier, N Larochette, PV Endert, F Ciccosanti, M Piacentini, L Zitvogel and G Kroemer. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nature Medicine 2007; 13, 54-61.
AG Lin, B Xiang, DJ Merlino, TR Baybutt, J Sahu, A Fridman, AE Snook and V Miller. Non-thermal plasma induces immunogenic cell death in vivo in murine CT26 colorectal tumors. Oncoimmunology 2018; 7(9), e1484978.
NE Sounni and A Noel. Targeting the tumor microenvironment for cancer therapy. Clinical Chemistry 2013; 59(1), 85-93.
A Privat-Maldonado, C Bengtson, J Razzokov, E Smits and A Bogaerts. Modifying the tumour microenvironment: Challenges and future perspectives for anticancer plasma treatments. Cancers 2019; 11(12), 1920.
M Weiss, D Gümbel, EM Hanschmann, R Mandelkow, N Gelbrich, U Zimmermann, R Walther, A Ekkernkamp, A Sckell, A Kramer, M Burchardt, CH Lillig and MB Stope. Cold atmospheric plasma treatment induces anti-proliferative effects in prostate cancer cells by redox and apoptotic signaling pathways. PLoS One 2015; 10(7), e0130350.
T Liu, C Han, S Wang, P Fang, Z Ma, L Xu and R Yin. Cancer-associated fibroblasts: An emerging target of anti-cancer immunotherapy. Journal of Hematology & Oncology 2019; 12, 86.
L Haralambiev, O Neuffer, A Nitsch, NC Kross, S Bekeschus, P Hinz, A Mustea, A Ekkernkamp, D Gümbel and MB Stope. Inhibition of angiogenesis by treatment with cold atmospheric plasma as a promising therapeutic approach in oncology. International Journal of Molecular Sciences 2020; 21, 7098.
S Bekeschus, R Clemen and HR Metelmann. Potentiating anti-tumor immunity with physical plasma. Clinical Plasma Medicine 2018; 12, 17-22.
S Bekeschus, K Rödder, B Fregin, O Otto, M Lippert, KD Weltmann, K Wende, A Schmidt and RK Gandhirajan. Toxicity and immunogenicity in murine melanoma following exposure to physical plasma-derived oxidants. Oxidative Medicine and Cellular Longevity 2017; 2017, 4396467.
MG Kong, M Keidar and K Ostrikov. Plasmas meet nanoparticles - where synergies can advance the frontier of medicine. Journal of Physics D: Applied Physics 2011; 44, 174018.
W Zhu, SJ Lee, NJ Castro, D Yan, M Keidar and LG Zhang. Synergistic effect of cold atmospheric plasma and drug loaded core-shell nanoparticles on inhibiting breast cancer cell growth. Scientific Reports 2016; 6, 21974.
A Jalili, S Irani and R Mirfakhraie. Combination of cold atmospheric plasma and iron nanoparticles in breast cancer: Gene expression and apoptosis study. OncoTargets and Therapy 2016; 2016(9), 5911-5917.
H Yu, Y Wang, S Wang, X Li, W Li, D Ding, X Gong, M Keidar and W Zhang. Paclitaxel-loaded core-shell magnetic nanoparticles and cold atmospheric plasma inhibit non-small cell lung cancer growth. ACS Applied Materials & Interfaces 2018; 10, 43462-43471.
E Manaloto, AA Gowen, A Lesniak, Z He, A Casey, PJ Cullen and JF Curtin. Cold atmospheric plasma induces silver nanoparticle uptake, oxidative dissolution and enhanced cytotoxicity in glioblastoma multiforme cells. Archives of Biochemistry and Biophysics 2020; 689, 108462.
GC Kim, GJ Kim, SR Park, SM Jeon, HJ Seo, F Iza and JK Lee. Air plasma coupled with antibody-conjugated nanoparticles: A new weapon against cancer. Journal of Physics D: Applied Physics 2009; 42, 32005.
X Cheng, W Murphy, N Recek, D Yan, U Cvelbar, A Vesel, M Mozetič, J Canady, M Keidar and JH Sherman. Synergistic effect of gold nanoparticles and cold plasma on glioblastoma cancer therapy. Journal of Physics D: Applied Physics 2014; 47, 335402.
NK Kaushik, N Kaushik, KC Yoo, N Uddin, JS Kim, SJ Lee and EH Choi. Low doses of PEG-coated gold nanoparticles sensitize solid tumors to cold plasma by blocking the PI3K/AKT-driven signaling axis to suppress cellular transformation by inhibiting growth and EMT. Biomaterials 2016; 87, 118-130.
G Daeschlein, A Hillmann, D Gumbel, C Sicher, SV Podewils, MB Stope and J Jünger. Enhanced anticancer efficacy by drug chemotherapy and cold atmospheric plasma against melanoma and glioblastoma cell lines. IEEE Transactions on Radiation and Plasma Medical Sciences 2018; 2(2), 153-159.
J Köritzer, V Boxhammer, A Schäfer, T Shimizu, TG Klämpfl, YF Li, C Welz, S Schwenk-Zieger, GE Morfill, JL Zimmermann nad J Schlegel. Restoration of sensitivity in chemo - resistant glioma cells by cold atmospheric plasma. PLoS One 2013; 8(5), e64498.
D Yan, JH Sherman and M Keidar. The application of the cold atmospheric plasma-activated solutions in cancer treatment. Anti-Cancer Agents in Medicinal Chemistry 2017; 18(6), 769-775.
NH Nguyen, HJ Park, SS Yang, KS Choi and JS Lee. Anti-cancer efficacy of nonthermal plasma dissolved in a liquid, liquid plasma in heterogeneous cancer cells. Scientific Reports 2016; 6, 29020.
S Bekeschus, A Käding, T Schröder, K Wende, C Hackbarth, KR Liedtke, JVD Linde, TV Woedtke, CD Heidecke and LI Partecke. Cold physical plasma-treated buffered saline solution as effective agent against pancreatic cancer cells. Anti-Cancer Agents in Medicinal Chemistry 2018; 18(6), 824-831.
L Wang, X Yang, C Yang, J Gao, Y Zhao, C Cheng, G Zhao and S Liu. The inhibition effect of cold atmospheric plasma-activated media in cutaneous squamous carcinoma cells. Future Oncology 2019; 15(5), 495-505.
M Adhikari, N Kaushik, B Ghimire, B Adhikari, S Baboota, AA Al-Khedhairy, R Wahab, SJ Lee, NK Kaushik and EH Choi. Cold atmospheric plasma and silymarin nanoemulsion synergistically inhibits human melanoma tumorigenesis via targeting HGF/c-MET downstream pathway. Cell Communication and Signaling 2019; 17, 52.
D Yan, Q Wang, M Adhikari, A Malyavko, L Lin, DB Zolotukhin, X Yao, M Kirschner, JH Sherman and M Keidar. A physically triggered cell death via transbarrier cold atmospheric plasma cancer treatment. ACS Applied Materials & Interfaces 2020; 12(31), 34548-34563.
G Isbary, W Stolz, T Shimizu, R Monetti, W Bunk, HU Schmidt, GE Morfill, TG Klämpfl, B Steffes, HM Thomas, J Heinlin, S Karrer, M Landthaler and JL Zimmermann. Cold atmospheric argon plasma treatment may accelerate wound healing in chronic wounds: Results of an open retrospective randomized controlled study in vivo. Clinical Plasma Medicine 2013; 1(2), 25-30.
J Gay-Mimbrera, MC García, B Isla-Tejera, A Rodero-Serrano, AV García-Nieto and J Ruano. Clinical and biological principles of cold atmospheric plasma application in skin cancer. Advances in Therapy 2016; 33, 894-909.
A Chuangsuwanich, T Assadamongkol and D Boonyawan. The healing effect of low-temperature atmospheric-pressure plasma in pressure ulcer: A randomized controlled trial. The International Journal of Lower Extremity Wounds 2016; 15(4), 313-319.
A Shashurin. Treat cancer with cold plasma: Produce aerospace engineer helps bring first clinical trial. 2019, Available at: https://www.purdue.edu/newsroom/releases/2019/Q3/treat-cancer-with-cold-plasma-produce-aerospace-engineer-helps-bring-first-clinical-trial.html, accessed May 2024.
A Shakya, HB Baniya, SP Pradhan, N Basnet, R Adhikari, DP Subedi and S Regmi. Cold plasma as a practical approach to cancer treatment. Plasma Medicine 2023; 12(4), 57-73.
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