journal article·2019-08-29Open access

Application of Non-Thermal Plasma on Biofilm: A Review

Tripti Thapa Gupta, Halim Ayan

Applied Sciences· Volume 9· Issue 17

Abstract

The formation of bacterial biofilm on implanted devices or damaged tissues leads to biomaterial-associated infections often resulting in life-threatening diseases and implant failure. It is a challenging process to eradicate biofilms as they are resistant to antimicrobial treatments. Conventional techniques, such as high heat and chemicals exposure, may not be suitable for biofilm removal in nosocomial settings. These techniques create surface degradation on the treated materials and lead to environmental pollution due to the use of toxic chemicals. A novel technique known as non-thermal plasma has a great potential to decontaminate or sterilize those nosocomial biofilms. This article aims to provide readers with an extensive review of non-thermal plasma and biofilms to facilitate further investigations. A brief introduction summarizes the problem caused by biofilms in hospital settings with current techniques used for biofilm inactivation followed by the literature review strategy. The remainder of the review discusses plasma and its generation, the role played by plasma reactive species, various factors affecting the antimicrobial efficacy of non-thermal plasma and summarizes many studies published in the field.
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Research context

OpenAlex topics: Plasma Applications and Diagnostics · Surface Modification and Superhydrophobicity · Electrospun Nanofibers in Biomedical Applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Bioengineering, College of Engineering, University of Toledo, Toledo, OH 43606, USA

Department of Mechanical, Industrial and Manufacturing Engineering, College of Engineering, University of Toledo, Toledo, OH 43606, USA

References (100+)

Show source-provided references
1. Biofilms and antibiotic therapy: Is there a role for combating bacterial resistance by the use of novel drug delivery systems?10.1016/j.addr.2005.04.007 ↗
2. Potential applications of nonthermal plasmas against biofilm-associated micro-organisms in vitro10.1111/jam.13404 ↗
3. Alkawareek, M.Y., Algwari, Q.T., Laverty, G., Gorman, S.P., Graham, W.G., O’Connell, D., and Gilmore, B.F. (2012). Eradication of Pseudomonas aeruginosa biofilms by atmospheric pressure non-thermal plasma. PLoS ONE, 7.10.1371/journal.pone.0044289 ↗
4. Antibiotic resistance of bacterial biofilms10.1016/j.ijantimicag.2009.12.011 ↗
5. Strategies for combating bacterial biofilm infections10.1038/ijos.2014.65 ↗
6. What You Should Know About Biofilm and Implants
7. The role of biofilms: Are we hitting the right target?10.1097/PRS.0b013e3181fca244 ↗
8. Current and emergent strategies for disinfection of hospital environments10.1093/jac/dkt281 ↗
9. Biofilms in device-related infections
10. Biofilms and device-associated infections10.3201/eid0702.010226 ↗
11. Dry mouth and denture plaque microflora in complete denture and palatal obturator prosthesis wearers10.1111/ger.12073 ↗
12. Prosthesis infections after orthopedic joint replacement: The possible role of bacterial biofilms
13. An organoselenium compound inhibits Staphylococcus aureus biofilms on hemodialysis catheters in vivo10.1128/AAC.05680-11 ↗
14. de Biofilm on artificial pacemaker: Fiction or reality?10.1590/S0066-782X2011001400018 ↗
15. Cold atmospheric pressure plasma and decontamination. Can it contribute to preventing hospital-acquired infections?10.1016/j.jhin.2014.06.015 ↗
16. Khan, M.S.A., Ahmad, I., Sajid, M., and Cameotra, S.S. (2014). Current and emergent control strategies for medical biofilms. Antibiofilm Agents, Springer.10.1007/978-3-642-53833-9_7 ↗
17. Rutala, W.A., and Weber, D.J. (2019, August 15). Guideline for Disinfection and Sterilization in Healthcare Facilities, Available online: http://www.cdc.gov/hicpac/pdf/guidelines/Disinfection_Nov_2008.pdf.
18. Contamination, disinfection, and cross-colonization: Are hospital surfaces reservoirs for nosocomial infection?10.1086/424667 ↗
19. Cold air plasma to decontaminate inanimate surfaces of the hospital environment10.1128/AEM.03480-13 ↗
20. Bacterial biofilms within the clinical setting: What healthcare professionals should know10.1016/j.jhin.2006.06.028 ↗
21. Fungal Biofilm & Medical Device Associated Infection: It’s Formation, Diagnosis & Future Trends: A Review
22. Challenges in biofilm inactivation: The use of cold plasma as a new approach
23. Biofilm formation: A clinically relevant microbiological process10.1086/322972 ↗
24. Biofilms in periprosthetic orthopedic infections10.2217/fmb.14.64 ↗
25. Developmental regulation of microbial biofilms10.1016/S0958-1669(02)00318-X ↗
26. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms10.1128/AEM.02073-07 ↗
27. The clinical impact of bacterial biofilms10.4248/IJOS11026 ↗
28. Mechanisms of biofilm resistance to antimicrobial agents10.1016/S0966-842X(00)01913-2 ↗
29. Antibiotic resistance of bacteria in biofilms10.1016/S0140-6736(01)05321-1 ↗
30. Killing of adherent oral microbes by a non-thermal atmospheric plasma jet10.1099/jmm.0.013714-0 ↗
31. Antimicrobial efficacy of non-thermal plasma in comparison to chlorhexidine against dental biofilms on titanium discs in vitro—Proof of principle experiment10.1111/j.1600-051X.2011.01740.x ↗
32. Gupta, T.T., and Ayan, H. (2017, January 21–25). Non-Thermal Plasma in Conjunction with Chlorhexidine (Chx) Digluconate Sterilize The Biofilm Contaminated Titanium Surface. Proceedings of the 2017 IEEE International Conference on Plasma Science (ICOPS), Atlantic City, NJ, USA.10.1109/PLASMA.2017.8496151 ↗
33. Gupta, T.T. (2018). Characterization and Optimization of Non-Thermal Plasma for Biofilm Sterilization. [Ph.D. Thesis, University of Toledo].
34. Generation and role of reactive oxygen and nitrogen species induced by plasma, lasers, chemical agents, and other systems in dentistry10.1155/2017/7542540 ↗
35. Bactericidal action of the reactive species produced by gas-discharge nonthermal plasma at atmospheric pressure: A review10.1109/TPS.2006.878381 ↗
36. The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology10.1088/0022-3727/45/26/263001 ↗
37. Non-thermal plasma technologies: New tools for bio-decontamination10.1016/j.biotechadv.2008.08.001 ↗
38. Cold Atmospheric Plasma: Methods of production and application in dentistry and oncology10.1186/2045-9912-3-21 ↗
39. Applied plasma medicine10.1002/ppap.200700154 ↗
40. Cold atmospheric plasma in cancer therapy10.1063/1.4801516 ↗
41. Ayan, H. (2009). Uniform Dielectric Barrier Discharge with Nanosecond Pulse Excitation for Biomedical Applications. [Ph.D. Thesis, Drexel University].
42. Augmented survival of Neisseria gonorrhoeae within biofilms: Exposure to atmospheric pressure non-thermal plasmas10.1007/s10096-010-1047-3 ↗
43. Cold plasma therapy of a tooth root canal infected with Enterococcus faecalis biofilms in vitro10.1016/j.joen.2012.08.017 ↗
44. Deactivation of Streptococcus mutans biofilms on a tooth surface using he dielectric barrier discharge at atmospheric pressure10.1088/1009-0630/15/6/09 ↗
45. Inactivation of Gram-positive biofilms by low-temperature plasma jet at atmospheric pressure10.1088/0022-3727/45/34/345202 ↗
46. How deep can plasma penetrate into a biofilm?10.1063/1.3597622 ↗
47. Control of methicillin-resistant Staphylococcus aureus in planktonic form and biofilms: A biocidal efficacy study of nonthermal dielectric-barrier discharge plasma10.1016/j.ajic.2009.11.002 ↗
48. Dielectric barrier discharge atmospheric cold plasma for inactivation of Pseudomonas aeruginosa biofilms10.1615/PlasmaMed.2014011996 ↗
49. Inactivation Effects of Non-Thermal Atmospheric-Pressure Helium Plasma Jet on Staphylococcus aureus Biofilms10.1002/ppap.201500006 ↗
50. Low power gas discharge plasma mediated inactivation and removal of biofilms formed on biomaterials10.1016/j.cap.2012.12.024 ↗
51. Bactericidal effects of non-thermal argon plasma in vitro, in biofilms and in the animal model of infected wounds10.1099/jmm.0.020263-0 ↗
52. Inactivation of biofilms using a low power atmospheric pressure argon plasma jet; the role of entrained nitrogen10.1002/ppap.201400074 ↗
53. Matthes, R., Bender, C., Schlüter, R., Koban, I., Bussiahn, R., Reuter, S., Lademann, J., Weltmann, K.D., and Kramer, A. (2013). Antimicrobial Efficacy of Two Surface Barrier Discharges with Air Plasma against In Vitro Biofilms. PLoS ONE, 8.10.1371/journal.pone.0070462 ↗
54. Treatment of Candida albicans biofilms with low-temperature plasma induced by dielectric barrier discharge and atmospheric pressure plasma jet10.1088/1367-2630/12/7/073039 ↗
55. Contact-free inactivation of Candida albicans biofilms by cold atmospheric air plasma10.1128/AEM.07235-11 ↗
56. Vandervoort, K.G., and Brelles-Mariño, G. (2014). Plasma-mediated inactivation of Pseudomonas aeruginosa biofilms grown on borosilicate surfaces under continuous culture system. PLoS ONE, 9.10.1371/journal.pone.0108512 ↗
57. Antimicrobial efficacy of an atmospheric pressure plasma jet against biofilms of Pseudomonas aeruginosa and Staphylococcus epidermidis10.1002/ppap.201100133 ↗
58. In Vitro Antimicrobial Effect of a Cold Plasma Jet against Enterococcus faecalis Biofilms
59. Application of atmospheric pressure nonthermal plasma for the in vitro eradication of bacterial biofilms10.1111/j.1574-695X.2012.00942.x ↗
60. Streptococci biofilm decontamination on teeth by low-temperature air plasma of dc corona discharges10.1088/0022-3727/47/22/224014 ↗
61. Fricke, K., Koban, I., Tresp, H., Jablonowski, L., Schröder, K., Kramer, A., Weltmann, K.D., von Woedtke, T., and Kocher, T. (2012). Atmospheric pressure plasma: A high-performance tool for the efficient removal of biofilms. PLoS ONE, 7.10.1371/journal.pone.0042539 ↗
62. Pseudomonas aeruginosa biofilm inactivation: Decreased cell culturability, adhesiveness to surfaces, and biofilm thickness upon high-pressure nonthermal plasma treatment10.1109/TPS.2010.2082570 ↗
63. Atmospheric pressure plasma jet for medical therapy: Plasma parameters and risk estimation10.1002/ctpp.200910067 ↗
64. The plasma jet kINPen—A powerful tool for wound healing10.1016/j.cpme.2016.01.001 ↗
65. Feed gas humidity: A vital parameter affecting a cold atmospheric-pressure plasma jet and plasma-treated human skin cells10.1088/0022-3727/46/29/295401 ↗
66. Randomized placebo-controlled human pilot study of cold atmospheric argon plasma on skin graft donor sites10.1111/wrr.12078 ↗
67. 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)10.1111/jdv.12490 ↗
68. Successful and safe use of 2 min cold atmospheric argon plasma in chronic wounds: Results of a randomized controlled trial10.1111/j.1365-2133.2012.10923.x ↗
69. Sterilization of Biofilm on a Titanium Surface Using a Combination of Nonthermal Plasma and Chlorhexidine Digluconate10.1155/2017/6085741 ↗
70. Antimicrobial Effectiveness of Regular Dielectric-Barrier Discharge (DBD) and Jet DBD on the Viability of Pseudomonas aeruginosa10.1109/TPS.2017.2748982 ↗
71. Application of nanosecond-pulsed dielectric barrier discharge for biomedical treatment of topographically non-uniform surfaces10.1088/0022-3727/42/12/125202 ↗
72. Blood coagulation and living tissue sterilization by floating-electrode dielectric barrier discharge in air10.1007/s11090-006-9024-4 ↗
73. Plasma medicine: An introductory review10.1088/1367-2630/11/11/115012 ↗
74. Low temperature plasma-based sterilization: Overview and state-of-the-art10.1002/ppap.200400078 ↗
75. Cold atmospheric argon plasma treatment may accelerate wound healing in chronic wounds: Results of an open retrospective randomized controlled study in vivo10.1016/j.cpme.2013.06.001 ↗
76. Nanosecond-pulsed uniform dielectric-barrier discharge10.1109/TPS.2008.917947 ↗
77. Bactericidal efficacy of dielectric barrier discharge plasma on methicillin-resistant staphylococcus aureus and Escherichia coli in planktonic phase and colonies in vitro10.1615/PlasmaMed.v5.i1.10 ↗
78. Plasma needle for in vivo medical treatment: Recent developments and perspectives10.1088/0963-0252/15/4/S03 ↗
79. Plasma treatment of dental cavities: A feasibility study10.1109/TPS.2004.832636 ↗
80. Floating electrode dielectric barrier discharge plasma in air promoting apoptotic behavior in melanoma skin cancer cell lines10.1007/s11090-007-9048-4 ↗
81. Investigation of non-thermal plasma effects on lung cancer cells within 3D collagen matrices10.1088/1361-6463/aa7b10 ↗
82. Miniature Dielectric Barrier Discharge Nonthermal Plasma Induces Apoptosis in Lung Cancer Cells and Inhibits Cell Migration10.1155/2017/8058307 ↗
83. Kamath, U., Rajasekhara, S., Nazar, N., and Sathar, A. (2016). Cold Atmospheric Plasma; Break Through in Dentistry—A Review. Paripex-Indian J. Res., 5.
84. The bright future of dentistry with cold plasma-review
85. Gas plasmas and plasma modified materials in medicine10.2478/v10136-009-0013-9 ↗
86. Nonthermal plasma—A tool for decontamination and disinfection10.1016/j.biotechadv.2015.01.002 ↗
87. Plasmas for medicine10.1016/j.physrep.2013.05.005 ↗
88. Dielectric-barrier discharges: Their history, discharge physics, and industrial applications10.1023/A:1022470901385 ↗
89. Low temperature atmospheric pressure plasma sources for microbial decontamination10.1088/0022-3727/44/1/013002 ↗
90. Recent Advances in the Research on Non-Equilibrium Atmospheric Pressure Plasma Jets10.1002/ppap.200600114 ↗
91. Atmospheric-pressure plasma technology10.1088/0741-3335/46/12B/006 ↗
92. Neuber, J.U. (2016). Non-Thermal Atmospheric-Pressure Plasma for Sterilization of Surfaces and Biofilms. [Master’s Thesis, Old Dominion University].
93. Plasma medicine—Current state of research and medical application10.1088/0741-3335/59/1/014031 ↗
94. Atmospheric pressure plasma jets: An overview of devices and new directions10.1088/0963-0252/24/6/064001 ↗
95. Cold atmospheric plasma devices for medical issues10.1586/erd.13.4 ↗
96. Gupta, T., Karki, S., Fournier, R., and Ayan, H. (2018). Mathematical Modelling of the Effects of Plasma Treatment on the Diffusivity of Biofilm. Appl. Sci., 8.10.3390/app8101729 ↗
97. Kieft, I.E. (2005). Plasma Needle: Exploring Biomedical Applications of Non-Thermal Plasmas, Technische Universiteit Eindhoven.
98. Inactivation mechanisms of non-thermal plasma on microbes: A review10.1016/j.foodcont.2016.12.021 ↗
99. Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli10.1128/AAC.01002-10 ↗
100. Kalghatgi, S.U. (2010). Mechanisms of Interaction of Non-Thermal Plasma with Living Cells, Drexel University.