The In-Vitro Activity of a Cold Atmospheric Plasma Device Utilizing Ambient Air against Bacteria and Biofilms Associated with Periodontal or Peri-Implant Diseases

Due to its antimicrobial and healing-promoting effects, the application of cold atmospheric plasma (CAP) appears to be a promising modality in various fields of general medicine and dentistry. The aim of the present study was to evaluate the antibacterial and anti-biofilm activity of a handheld device utilizing ambient air for plasma generation. Suspensions of 11 oral bacteria (among them Fusobacterium nucleatum, Porphyromonas gingivalis, Parvimonas micra, Streptococcus gordonii, and Tannerella forsythia) were exposed to CAP for 10, 30, 60, and 120 s. Before and after treatment, colony forming unit (CFU) counts were determined. Then, 12-species biofilms were cultured on dentin and titanium specimens, and CAP was applied for 30, 60, and 120 s before quantifying CFU counts, biofilm mass, and metabolic activity. A reduction of ≥3 log10 CFU, was found for ten out of the eleven tested species at 30 s (except for T. forsythia) and for all species at 60 s. For biofilm grown on dentin and titanium specimens, the log10 reductions were 2.43 log10 CFU/specimen and by about 4 log10 CFU/specimen after 120 s of CAP. The CAP application did not reduce the biomass significantly, the metabolic activity of the biofilms on dentin and titanium decreased by 98% and 95% after 120 s of CAP. An application of 120 s of CAP had no cytotoxic effect on gingival fibroblasts and significantly increased the adhesion of gingival fibroblasts to the titanium surface. These results are promising and underline the potential of CAP for implementation in periodontal and peri-implantitis therapy.

[1]  A. Sculean,et al.  A novel in vitro periodontal pocket model to evaluate the effect of root surface instrumentation on biofilm-epithelial cell interactions , 2022, Clinical Oral Investigations.

[2]  B. Holtfreter,et al.  Efficiency of cold atmospheric plasma, cleaning powders and their combination for biofilm removal on two different titanium implant surfaces , 2022, Clinical oral investigations.

[3]  Alan D. Lopez,et al.  Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis , 2022, The Lancet.

[4]  Ming Yan,et al.  Effects of a Novel Cold Atmospheric Plasma Treatment of Titanium on the Proliferation and Adhesion Behavior of Fibroblasts , 2021, International journal of molecular sciences.

[5]  M. Suar,et al.  Aurora Borealis in dentistry: The applications of cold plasma in biomedicine , 2021, Materials today. Bio.

[6]  C. Mayer,et al.  Peptidoglycan Salvage Enables the Periodontal Pathogen Tannerella forsythia to Survive within the Oral Microbial Community , 2021, Microbial Physiology.

[7]  R. Fimmers,et al.  Prevalence and antibiotic susceptibility trends of periodontal pathogens in the subgingival microbiota of German periodontitis patients: A retrospective surveillance study. , 2021, Journal of clinical periodontology.

[8]  K. Ostrikov,et al.  Cold atmospheric plasma coupled with air abrasion in liquid medium for the treatment of peri-implantitis model grown with a complex human biofilm: an in vitro study , 2021, Clinical Oral Investigations.

[9]  A. Stratakos,et al.  Inactivation of Listeria monocytogenes and Salmonella on Stainless Steel by a Piezoelectric Cold Atmospheric Plasma Generator , 2021, Applied Sciences.

[10]  Xinpei Lu,et al.  In vitro and in vivo research of atmosphere pressure nonequilibrium plasmas on root canal disinfection: implication for alternative strategy for irrigation , 2021, Clinical Oral Investigations.

[11]  R. Darveau,et al.  Oral biofilms revisited: A novel host tissue of bacteriological origin. , 2021, Periodontology 2000.

[12]  G. Kotsakis,et al.  Peri-implantitis is not periodontitis: Scientific discoveries shed light on microbiome-biomaterial interactions that may determine disease phenotype. , 2021, Periodontology 2000.

[13]  M. Curtis,et al.  Microbial transitions from health to disease. , 2021, Periodontology 2000.

[14]  M. Al‐Rubeai,et al.  Cold atmospheric plasma as an interface biotechnology for enhancing surgical implants , 2021, Critical reviews in biotechnology.

[15]  E. Middelkoop,et al.  Antibacterial and safety tests of a flexible cold atmospheric plasma device for the stimulation of wound healing , 2021, Applied Microbiology and Biotechnology.

[16]  A. Sculean,et al.  The Antimicrobial Effect of Cold Atmospheric Plasma against Dental Pathogens—A Systematic Review of In-Vitro Studies , 2021, Antibiotics.

[17]  S. Nettesheim,et al.  Piezoelectric Direct Discharge: Devices and Applications , 2020, Plasma.

[18]  K. Ostrikov,et al.  Novel technique using cold atmospheric plasma coupled with air-polishing for the treatment of titanium discs grown with biofilm: An in-vitro study. , 2020, Dental materials : official publication of the Academy of Dental Materials.

[19]  Xincai Zhou,et al.  Evaluation of Modified Cold-Atmospheric Pressure Plasma (MCAP) for the Treatment of Peri-implantitis in Beagles. , 2020, Oral diseases.

[20]  D. Apatzidou,et al.  Understanding the microbial components of periodontal diseases and periodontal treatment-induced microbiological shifts. , 2020, Journal of medical microbiology.

[21]  K. Weltmann,et al.  Piezoelectric-driven plasma pen with multiple nozzles used as a medical device: risk estimation and antimicrobial efficacy , 2020, Journal of Physics D: Applied Physics.

[22]  Hom-lay Wang,et al.  Breaking the wave of peri-implantitis. , 2020, Periodontology 2000.

[23]  A. Piattelli,et al.  The Emerging Role of Cold Atmospheric Plasma in Implantology: A Review of the Literature , 2020, Nanomaterials.

[24]  B. Stratmann,et al.  Effect of Cold Atmospheric Plasma Therapy vs Standard Therapy Placebo on Wound Healing in Patients With Diabetic Foot Ulcers , 2020, JAMA network open.

[25]  P. Diaz,et al.  The role of the microbiota in periodontal disease. , 2020, Periodontology 2000.

[26]  Yifan Rao,et al.  Fighting Mixed-Species Microbial Biofilms With Cold Atmospheric Plasma , 2020, Frontiers in Microbiology.

[27]  I. Chapple,et al.  Treatment of stage I–III periodontitis—The EFP S3 level clinical practice guideline , 2020, Journal of clinical periodontology.

[28]  T. Sekino,et al.  Enhanced Osseointegration and Bio-Decontamination of Nanostructured Titanium Based on Non-Thermal Atmospheric Pressure Plasma , 2020, International journal of molecular sciences.

[29]  E. Halasová,et al.  Cold Atmospheric Plasma: A Powerful Tool for Modern Medicine , 2020, International journal of molecular sciences.

[30]  W. Teughels,et al.  Adjunctive effect of systemic antimicrobials in periodontitis therapy. A systematic review and meta-analysis. , 2020, Journal of clinical periodontology.

[31]  O. Karaman,et al.  Evaluation of efficacy of non-thermal atmospheric pressure plasma in treatment of periodontitis: a randomized controlled clinical trial , 2020, Clinical Oral Investigations.

[32]  S. Reese,et al.  In vitro evaluation of the decontamination effect of cold atmospheric argon plasma on selected bacteria frequently encountered in small animal bite injuries. , 2020, Journal of microbiological methods.

[33]  A. Valm,et al.  Microbial Interactions in Oral Communities Mediate Emergent Biofilm Properties , 2020, Journal of dental research.

[34]  M. Feres,et al.  Does subgingival bacterial colonization differ between implants and teeth? A systematic review. , 2019, Brazilian oral research.

[35]  Ji-Yoon Lee,et al.  The bactericidal effect of an atmospheric-pressure plasma jet on Porphyromonas gingivalis biofilms on sandblasted and acid-etched titanium discs , 2019, Journal of periodontal & implant science.

[36]  A. Quaranta,et al.  Prescribing trends of systemic antibiotics by periodontists in Australia. , 2019, Journal of periodontology.

[37]  C. Timon,et al.  Thermal Osteonecrosis Caused by Bone Drilling in Orthopedic Surgery: A Literature Review , 2019, Cureus.

[38]  Zhi Gao,et al.  Emission rates of indoor ozone emission devices: A literature review , 2019, Building and Environment.

[39]  S. Pushalkar,et al.  Low-temperature plasma on peri-implant-related biofilm and gingival tissue. , 2018, Journal of periodontology.

[40]  E. Choi,et al.  The Effects of Non-Thermal Atmospheric Pressure Plasma treated Titanium Surface on Behaviors of Oral Soft Tissue Cells , 2018, Scientific Reports.

[41]  Meng Chen,et al.  Non-thermal plasma reduces periodontitis-induced alveolar bone loss in rats. , 2018, Biochemical and biophysical research communications.

[42]  S. Laurencin-Dalicieux,et al.  Use of cold-atmospheric plasma in oncology: a concise systematic review , 2018, Therapeutic advances in medical oncology.

[43]  A. Burkovski,et al.  Argon Cold Plasma-A Novel Tool to Treat Therapy-resistant Corneal Infections. , 2018, American journal of ophthalmology.

[44]  I. Polyzois,et al.  Treatment of pathologic peri‐implant pockets , 2018, Periodontology 2000.

[45]  Jue Zhang,et al.  A novel cold atmospheric pressure air plasma jet for peri-implantitis treatment: An in vitro study. , 2018, Dental materials journal.

[46]  A. Sculean,et al.  Activity of taurolidine gels on ex vivo periodontal biofilm , 2018, Clinical Oral Investigations.

[47]  A. Cochis,et al.  Cold atmospheric plasma treatment affects early bacterial adhesion and decontamination of soft reline palatal obturators , 2017 .

[48]  B. Holtfreter,et al.  Removal of naturally grown human biofilm with an atmospheric pressure plasma jet: An in‐vitro study , 2017, Journal of biophotonics.

[49]  P. Marsh,et al.  Dental biofilm: ecological interactions in health and disease , 2017, Journal of clinical periodontology.

[50]  Praveen Sharma,et al.  Global epidemiology of dental caries and severe periodontitis – a comprehensive review , 2017, Journal of clinical periodontology.

[51]  Linfeng Wu,et al.  Effects of atmospheric non-thermal argon/oxygen plasma on biofilm viability and hydrophobicity of oral bacteria. , 2017, American journal of dentistry.

[52]  G. Donnarumma,et al.  Bacterial inactivation/sterilization by argon plasma treatment on contaminated titanium implant surfaces:In vitro study , 2015, Medicina oral, patologia oral y cirugia bucal.

[53]  Birte Holtfreter,et al.  Cold atmospheric plasma in combination with mechanical treatment improves osteoblast growth on biofilm covered titanium discs. , 2015, Biomaterials.

[54]  Xinpei Lu,et al.  Effects of non-equilibrium plasma in the treatment of ligature-induced peri-implantitis. , 2015, Journal of clinical periodontology.

[55]  S. Nietzsche,et al.  In-vitro activity of taurolidine on single species and a multispecies population associated with periodontitis. , 2015, Anaerobe.

[56]  R. Genco,et al.  Primary prevention of peri-implantitis: managing peri-implant mucositis. , 2015, Journal of clinical periodontology.

[57]  E. Choi,et al.  Air atmospheric-pressure plasma-jet treatment enhances the attachment of human gingival fibroblasts for early peri-implant soft tissue seals on titanium dental implant abutments , 2015, Acta odontologica Scandinavica.

[58]  J. Lackmann,et al.  Inactivation of microbes and macromolecules by atmospheric-pressure plasma jets , 2014, Applied Microbiology and Biotechnology.

[59]  T. Coenye,et al.  Optimization of resazurin-based viability staining for quantification of microbial biofilms. , 2014, Journal of microbiological methods.

[60]  A. Kramer,et al.  Antimicrobial efficacy of non-thermal plasma in comparison to chlorhexidine against dental biofilms on titanium discs in vitro - proof of principle experiment. , 2011, Journal of clinical periodontology.

[61]  T. Opperman,et al.  Static Biofilm Cultures of Gram‐Positive Pathogens Grown in a Microtiter Format Used for Anti‐Biofilm Drug Discovery , 2010, Current protocols in pharmacology.

[62]  Josselin Noirel,et al.  A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia , 2010, Proteomics.

[63]  B. Millar,et al.  Assessment of the safety of two ozone delivery devices. , 2007, Journal of dentistry.

[64]  L. Sabath,et al.  Clinical relevance of bacteriostatic versus bactericidal mechanisms of action in the treatment of Gram-positive bacterial infections. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[65]  Isao Ishikawa,et al.  Effects of the Er:YAG laser irradiation on titanium implant materials and contaminated implant abutment surfaces. , 2003, Journal of clinical laser medicine & surgery.

[66]  J. Escamilla,et al.  The aerobic electron transport system of Eikenella corrodens. , 2002, Canadian journal of microbiology.

[67]  C. Barclay,et al.  A pilot study of intraoral temperature changes , 2000, Clinical Oral Investigations.

[68]  H. Katz,et al.  Solid state magnetic and dielectric devices , 1959 .