Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
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Safety evaluation of atmospheric pressure plasma jets in in vitro and in vivo experiments

  • Lee, Ji-Yoon (Department of Periodontology and Dental Research Institute, School of Dentistry, Seoul National University) ;
  • Park, Shin-Young (Department of Dental Science and Dental Research Institute, School of Dentistry, Seoul National University) ;
  • Kim, Kyoung-Hwa (Department of Periodontology and Dental Research Institute, School of Dentistry, Seoul National University) ;
  • Yoon, Sung-Young (Plasma Technology Research Center, National Fusion Research Institute) ;
  • Kim, Gon-Ho (Department of Energy Systems (Nuclear) Engineering, Seoul National University School of Engineering) ;
  • Lee, Yong-Moo (Department of Periodontology and Dental Research Institute, School of Dentistry, Seoul National University) ;
  • Seol, Yang-Jo (Department of Periodontology and Dental Research Institute, School of Dentistry, Seoul National University)
  • Received : 2020.11.20
  • Accepted : 2021.03.05
  • Published : 2021.06.30
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Abstract

Purpose: The atmospheric pressure plasma jet (APPJ) has been introduced as an effective disinfection method for titanium surfaces due to their massive radical generation at low temperatures. Helium (He) has been widely applied as a discharge gas in APPJ due to its bactericidal effects and was proven to be effective in our previous study. This study aimed to evaluate the safety and effects of He-APPJ application at both the cell and tissue levels. Methods: Cellular-level responses were examined using human gingival fibroblasts and osteoblasts (MC3T3-E1 cells). He-APPJ was administered to the cells in the experimental group, while the control group received only He-gas treatment. Immediate cell responses and recovery after He-APPJ treatment were examined in both cell groups. The effect of He-APPJ on osteogenic differentiation was evaluated via an alkaline phosphatase activity assay. In vivo, He-APPJ treatment was administered to rat calvarial bone and the adjacent periosteum, and samples were harvested for histological examination. Results: He-APPJ treatment for 5 minutes induced irreversible effects in both human gingival fibroblasts and osteoblasts in vitro. Immediate cell detachment of human gingival fibroblasts and osteoblasts was shown regardless of treatment time. However, the detached areas in the groups treated for 1 or 3 minutes were completely repopulated within 7 days. Alkaline phosphatase activity was not influenced by 1 or 3 minutes of plasma treatment, but was significantly lower in the 5 minute-treated group (P=0.002). In vivo, He-APPJ treatment was administered to rat calvaria and periosteum for 1 or 3 minutes. No pathogenic changes occurred at 7 days after He-APPJ treatment in the He-APPJ-treated group compared to the control group (He gas only). Conclusions: Direct He-APPJ treatment for up to 3 minutes showed no harmful effects at either the cell or tissue level.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (NRF2020R1A2C1007536). This work was supported by the Research Resettlement Fund for new faculty, the Creative-Pioneering Researchers Program of Seoul National University.

References

  1. Heitz-Mayfield LJ, Lang NP. Comparative biology of chronic and aggressive periodontitis vs. periimplantitis. Periodontol 2000 2010;53:167-81. https://doi.org/10.1111/j.1600-0757.2010.00348.x
  2. Zhu B, Meng H, Huang B, Chen Z, Lu R. Detection of T. forsythia and other important bacteria in crestal and subcrestal implants with ligature-induced peri-implant infection in dogs. J Periodontol 2019;90:306-13. https://doi.org/10.1002/JPER.18-0223
  3. Mombelli A, Lang NP. The diagnosis and treatment of peri-implantitis. Periodontol 2000 1998;17:63-76. https://doi.org/10.1111/j.1600-0757.1998.tb00124.x
  4. Ehlbeck J, Brandenburg R, von Woedtke T, Krohmann U, Stieber M, Weltmann KD. PLASMOSE - antimicrobial effects of modular atmospheric plasma sources. GMS Krankenhhyg Interdiszip 2008;3:Doc14.
  5. Yonson S, Coulombe S, Leveille V, Leask R. Cell treatment and surface functionalization using a miniature atmospheric pressure glow discharge plasma torch. J Phys D Appl Phys 2006;39:3508-13. https://doi.org/10.1088/0022-3727/39/16/S08
  6. Lupu AR, Georgescu N, Calugaru A, Cremer L, Szegli G, Kerek F. The effects of cold atmospheric plasma jets on B16 and COLO320 tumoral cells. Roum Arch Microbiol Immunol 2009;68:136-44.
  7. Mendis DA, Rosenberg M, Azam F. A note on the possible electrostatic disruption of bacteria. IEEE Trans Plasma Sci 2000;28:1304-6. https://doi.org/10.1109/27.893321
  8. Laroussi M. Nonthermal decontamination of biological media by atmospheric-pressure plasmas: review, analysis, and prospects. IEEE Trans Plasma Sci 2002;30:1409-15. https://doi.org/10.1109/TPS.2002.804220
  9. Montie TC, Roth R. An overview of research using the one atmosphere uniform glow discharge plasma for sterilization of surfaces and materials. IEEE Trans Plasma Sci 2000;28:41-50. https://doi.org/10.1109/27.842860
  10. Kim JH, Lee MA, Han GJ, Cho BH. Plasma in dentistry: a review of basic concepts and applications in dentistry. Acta Odontol Scand 2014;72:1-12. https://doi.org/10.3109/00016357.2013.795660
  11. Guerrero-Preston R, Ogawa T, Uemura M, Shumulinsky G, Valle BL, Pirini F, et al. Cold atmospheric plasma treatment selectively targets head and neck squamous cell carcinoma cells. Int J Mol Med 2014;34:941-6. https://doi.org/10.3892/ijmm.2014.1849
  12. Lee JY, Kim KH, Park SY, Yoon SY, Kim GH, Lee YM, et al. The bactericidal effect of an atmospheric-pressure plasma jet on Porphyromonas gingivalis biofilms on sandblasted and acid-etched titanium discs. J Periodontal Implant Sci 2019;49:319-29. https://doi.org/10.5051/jpis.2019.49.5.319
  13. Yoon SY, Kim KH, Seol YJ, Kim SJ, Bae B, Huh SR, et al. Effects of metastable species in helium and argon atmospheric pressure plasma jets (APPJs) on inactivation of periodontopathogenic bacteria. J Korean Phys Soc 2016;68:1176-91. https://doi.org/10.3938/jkps.68.1176
  14. Park SY, Kim KH, Shin SY, Koo KT, Lee YM, Seol YJ. Dual delivery of rhPDGF-BB and bone marrow mesenchymal stromal cells expressing the BMP2 gene enhance bone formation in a critical-sized defect model. Tissue Eng Part A 2013;19:2495-505. https://doi.org/10.1089/ten.tea.2012.0648
  15. Kalghatgi S, Kelly CM, Cerchar E, Torabi B, Alekseev O, Fridman A, et al. Effects of non-thermal plasma on mammalian cells. PLoS One 2011;6:e16270. https://doi.org/10.1371/journal.pone.0016270
  16. Stoffels E, Sakiyama Y, Graves DB. Cold atmospheric plasma: charged species and their interactions with cells and tissues. IEEE Trans Plasma Sci 2008;36:1441-57. https://doi.org/10.1109/TPS.2008.2001084
  17. Volotskova O, Shashurin A, Stepp MA, Pal-Ghosh S, Keidar M. Plasma-controlled cell migration: localization of cold plasma-cell interaction region. Plasma Med 2011;1:85-92. https://doi.org/10.1615/PlasmaMed.v1.i1.70
  18. Virard F, Cousty S, Cambus JP, Valentin A, Kemoun P, Clement F. Cold atmospheric plasma induces a predominantly necrotic cell death via the microenvironment. PLoS One 2015;10:e0133120. https://doi.org/10.1371/journal.pone.0133120
  19. Stoffels E, Roks AJM, Deelman LE. Delayed effects of cold atmospheric plasma on vascular cells. Plasma Process Polym 2008;5:599-605. https://doi.org/10.1002/ppap.200800028
  20. Canal C, Fontelo R, Hamouda I, Guillem-Marti J, Cvelbar U, Ginebra MP. Plasma-induced selectivity in bone cancer cells death. Free Radic Biol Med 2017;110:72-80. https://doi.org/10.1016/j.freeradbiomed.2017.05.023
  21. Bender C, Matthes R, Kindel E, Kramer A, Lademann J, Weltmann KD, et al. The irritation potential of nonthermal atmospheric pressure plasma in the HET-CAM. Plasma Process Polym 2010;7:318-26. https://doi.org/10.1002/ppap.200900119
  22. Fridman G, Friedman G, Gutsol A, Shekhter AB, Vasilets VN, Fridman A. Applied plasma medicine. Plasma Process Polym 2008;5:503-33. https://doi.org/10.1002/ppap.200700154
  23. Ermolaeva SA, Varfolomeev AF, Chernukha MY, Yurov DS, Vasiliev MM, Kaminskaya AA, et al. Bactericidal effects of non-thermal argon plasma in vitro, in biofilms and in the animal model of infected wounds. J Med Microbiol 2011;60:75-83. https://doi.org/10.1099/jmm.0.020263-0
  24. Nastuta AV, Topala I, Grigoras C, Pohoata V, Popa G. Stimulation of wound healing by helium atmospheric pressure plasma treatment. J Phys D Appl Phys 2011;44:105204. https://doi.org/10.1088/0022-3727/44/10/105204
  25. Shashurin A, Keidar M, Bronnikov S, Jurjus RA, Stepp MA. Living tissue under treatment of cold plasma atmospheric jet. Appl Phys Lett 2008;93:181501. https://doi.org/10.1063/1.3020223
  26. Kieft IE, Broers JL, Caubet-Hilloutou V, Slaaf DW, Ramaekers FC, Stoffels E. Electric discharge plasmas influence attachment of cultured CHO K1 cells. Bioelectromagnetics 2004;25:362-8. https://doi.org/10.1002/bem.20005
  27. Xu D, Luo X, Xu Y, Cui Q, Yang Y, Liu D, et al. The effects of cold atmospheric plasma on cell adhesion, differentiation, migration, apoptosis and drug sensitivity of multiple myeloma. Biochem Biophys Res Commun 2016;473:1125-32. https://doi.org/10.1016/j.bbrc.2016.04.027
  28. Fridman G, Shereshevsky A, Jost MM, Brooks AD, Fridman A, Gutsol A, et al. Floating electrode dielectric barrier discharge plasma in air promoting apoptotic behavior in melanoma skin cancer cell lines. Plasma Chem Plasma Process 2007;27:163-76. https://doi.org/10.1007/s11090-007-9048-4
  29. Lee JH, Kim KN. Effects of a nonthermal atmospheric pressure plasma jet on human gingival fibroblasts for biomedical application. BioMed Res Int 2016;2016:2876916. https://doi.org/10.1155/2016/2876916
  30. Kieft IE, Darios D, Roks AJM, Stoffels E. Plasma treatment of mammalian vascular cells: a quantitative description. IEEE Trans Plasma Sci 2005;33:771-5. https://doi.org/10.1109/TPS.2005.844528
  31. Fridman G, Shereshevsky A, Peddinghaus M, Gutsol A, Vasilets V, Brooks A, et al. Bio-medical applications of non-thermal atmospheric pressure plasma. In Proceedings of the 37th AIAA Plasmadynamics and Lasers Conference; 2006 Jun 5-8; San Francisco, CA. Reston, VA: American Institute of Aeronautics and Astronautics; 2006.
  32. Fridman G, Peddinghaus M, Balasubramanian M, Ayan H, Fridman A, Gutsol A, et al. Blood coagulation and living tissue sterilization by floating-electrode dielectric barrier discharge in air. Plasma Chem Plasma Process 2006;26:425-42. https://doi.org/10.1007/s11090-006-9024-4
  33. Wu AS, Kalghatgi S, Dobrynin D, Sensenig R, Cerchar E, Podolsky E, et al. Porcine intact and wounded skin responses to atmospheric nonthermal plasma. J Surg Res 2013;179:e1-12. https://doi.org/10.1016/j.jss.2012.02.039
  34. Liu D, Xiong Z, Du T, Zhou X, Cao Y, Lu X. Bacterial-killing effect of atmospheric pressure non-equilibrium plasma jet and oral mucosa response. J Huazhong Univ Sci Technolog Med Sci 2011;31:852-6. https://doi.org/10.1007/s11596-011-0690-y