{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T20:31:44Z","timestamp":1790109104658,"version":"4.0.1"},"reference-count":56,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2025,4,5]],"date-time":"2025-04-05T00:00:00Z","timestamp":1743811200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"NIH","award":["1R21DE031868-01A1"],"award-info":[{"award-number":["1R21DE031868-01A1"]}]},{"name":"University of Missouri, School of Medicine, Department of Internal Medicine RIF fund","award":["1R21DE031868-01A1"],"award-info":[{"award-number":["1R21DE031868-01A1"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JFB"],"abstract":"<jats:p>The objective of this study was an assessment of the anti-biofilm properties of fluoride non-thermal atmospheric plasma (FNTAP) generated using argon and hydrocarbon fluoride gas 1,1,1,2-tetrafluoroethane (TFE). These properties were evaluated by measuring the destruction and recovery of in vitro dual-species biofilms of Streptococcus mutans and Streptococcus sanguinis exposed to FNTAP at 5 or 10 standard cubic centimeters per minute (sccm) or argon non-thermal atmospheric plasma (ArNTAP) for 1 or 2 min, using resazurin-based reagent viability assays, colony forming units (CFU), culture media pH and live\/dead staining. Both ArNTAP and FNTAP resulted in significant immediate reductions in bacterial load as compared to the control. Although ArNTAP did not significantly reduce biofilm regrowth, FNTAP treatment showed a bacterial load reduction of more than 5 log units of biofilm regrowth. FNTAP treatments significantly reduced the acidification of the culture medium after recovery incubation, indicating reduced living bacteria, with a pH of 6.92 \u00b1 0.02 and 6.90 \u00b1 0.03, respectively, for the 5 sccm and 10 sccm FNTAP treatments, as compared to a pH of 5.83 \u00b1 0.26 for the ArNTAP treatment, and a significantly acidic pH of 4.76 \u00b1 0.04 for the no-treatment groups. Our results suggest that FNTAP has exceptional anti-biofilm effects, and future directions of our research include the assessment of potential applications of FNTAP in clinical settings.<\/jats:p>","DOI":"10.3390\/jfb16040132","type":"journal-article","created":{"date-parts":[[2025,4,7]],"date-time":"2025-04-07T03:23:07Z","timestamp":1743996187000},"page":"132","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Non-Thermal Atmospheric Plasma Enhances Biological Effects of Fluoride on Oral Biofilms"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6321-7800","authenticated-orcid":false,"given":"Anushri","family":"Warang","sequence":"first","affiliation":[{"name":"Department of Internal Medicine, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isha","family":"Deol","sequence":"additional","affiliation":[{"name":"Department of Chemical and Biomedical Engineering, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Fakher","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linfeng","family":"Wu","sequence":"additional","affiliation":[{"name":"Department of Public Health Sciences, College of Dentistry, Texas A&M University, Dallas, TX 75246, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liang","family":"Hong","sequence":"additional","affiliation":[{"name":"Department of Public Health Sciences, College of Dentistry, Texas A&M University, Dallas, TX 75246, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shaoping","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Periodontics, College of Dentistry, University of Iowa, Iowa City, IA 52242, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingsong","family":"Yu","sequence":"additional","affiliation":[{"name":"Department of Mechanical and Aerospace Engineering, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4545-2417","authenticated-orcid":false,"given":"Hongmin","family":"Sun","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, University of Missouri, Columbia, MO 65211, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,4,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1177\/0022034513490168","article-title":"Global burden of oral conditions in 1990-2010: A systematic analysis","volume":"92","author":"Marcenes","year":"2013","journal-title":"J. Dent. Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2163","DOI":"10.1016\/S0140-6736(12)61729-2","article-title":"Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990\u20132010: A systematic analysis for the Global Burden of Disease Study 2010","volume":"380","author":"Vos","year":"2012","journal-title":"Lancet"},{"key":"ref_3","first-page":"1781","article-title":"Awareness Among Dental Students On Strategies Over Early Childhood Caries","volume":"12","author":"Ushanthika","year":"2020","journal-title":"Int. J. Pharm. Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1111\/j.1752-7325.1998.tb03007.x","article-title":"Fluoride Varnish: A Useful New Tool for Public Health Dentistry","volume":"58","author":"Bawden","year":"1998","journal-title":"J. Public Health Dent."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"9120","DOI":"10.37506\/ijfmt.v14i4.13167","article-title":"Topical Fluoride for Prevention of Dental Caries: A Review","volume":"14","author":"Nayak","year":"2020","journal-title":"Indian J. Forensic Med. Toxicol."},{"key":"ref_6","first-page":"37","article-title":"Use of fluorides in dental caries management","volume":"58","author":"Chu","year":"2010","journal-title":"Gen. Dent."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Gao, S.S., Zhang, S., Mei, M.L., Lo, E.C., and Chu, C.H. (2016). Caries remineralisation and arresting effect in children by professionally applied fluoride treatment\u2014A systematic review. BMC Oral Health, 16.","DOI":"10.1186\/s12903-016-0171-6"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1111\/j.1600-0722.1997.tb00231.x","article-title":"Review on fluoride, with special emphasis on calcium fluoride mechanisms in caries prevention","volume":"105","year":"1997","journal-title":"Eur. J. Oral Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1159\/000325151","article-title":"Mechanisms of action of fluoride for caries control","volume":"22","author":"Buzalaf","year":"2011","journal-title":"Monogr. Oral Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1177\/154407370802000105","article-title":"Strategies to enhance the biological effects of fluoride on dental biofilms","volume":"20","author":"Koo","year":"2008","journal-title":"Adv. Dent. Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1177\/00220345900690S127","article-title":"Effects of Fluoride on the Microbial Ecology of Dental Plaque","volume":"69","author":"Bowden","year":"1990","journal-title":"J. Dent. Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1244","DOI":"10.1177\/00220345900690060401","article-title":"Biochemical mechanisms of enhanced inhibition of fluoride on the anaerobic sugar metabolism by Streptococcus sanguis","volume":"69","author":"Hata","year":"1990","journal-title":"J. Dent. Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1177\/00220345900690S128","article-title":"Biochemical effects of fluoride on oral bacteria","volume":"69","author":"Hamilton","year":"1990","journal-title":"J. Dent. Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1111\/j.1574-6968.2005.00018.x","article-title":"Co-operative inhibition by fluoride and zinc of glucosyl transferase production and polysaccharide synthesis by mutans streptococci in suspension cultures and biofilms","volume":"254","author":"Koo","year":"2006","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1111\/odi.12407","article-title":"Short-term effects of povidone iodine and sodium fluoride therapy on plaque levels and microbiome diversity","volume":"22","author":"Reilly","year":"2016","journal-title":"Oral Dis."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Koopman, J.E., van der Kaaij, N.C., Buijs, M.J., Elyassi, Y., van der Veen, M.H., Crielaard, W., Ten Cate, J.M., and Zaura, E. (2015). The Effect of Fixed Orthodontic Appliances and Fluoride Mouthwash on the Oral Microbiome of Adolescents\u2014A Randomized Controlled Clinical Trial. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0137318"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"179","DOI":"10.5644\/ama2006-124.85","article-title":"The cariostatic mechanisms of fluoride","volume":"42","author":"Sutej","year":"2013","journal-title":"Acta. Med. Acad."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.archoralbio.2018.02.010","article-title":"Effect of sodium fluoride on oral biofilm microbiota and enamel demineralization","volume":"89","author":"Thurnheer","year":"2018","journal-title":"Arch. Oral Biol."},{"key":"ref_19","first-page":"121","article-title":"Fluoride in the environment and its metabolism in humans","volume":"211","author":"Jha","year":"2011","journal-title":"Rev. Environ. Contam. Toxicol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Shen, Y., Yu, F., Qiu, L., Gao, M., Xu, P., Zhang, L., Liao, X., Wang, M., Hu, X., and Sun, Y. (2022). Ecological influence by colonization of fluoride-resistant Streptococcus mutans in oral biofilm. Front. Cell Infect. Microbiol., 12.","DOI":"10.3389\/fcimb.2022.1106392"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1007\/s40572-020-00270-9","article-title":"Fluoride in Drinking Water and Skeletal Fluorosis: A Review of the Global Impact","volume":"7","author":"Srivastava","year":"2020","journal-title":"Curr. Environ. Health Rep."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1177\/00220345800590021501","article-title":"Fluoride resistance and adherence of selected strains of Streptococcus mutans to smooth surfaces after exposure to fluoride","volume":"59","author":"Streckfuss","year":"1980","journal-title":"J. Dent. Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1177\/00220345830620061201","article-title":"Effect of continuous fluoride gel use on plaque fluoride retention and microbial activity","volume":"62","author":"Brown","year":"1983","journal-title":"J. Dent. Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1491","DOI":"10.1177\/00220345910700120401","article-title":"In vitro demineralization of enamel by F-sensitive and F-resistant mutans streptococci in the presence of 0, 0.05, or 0.5 mmol\/L NaF","volume":"70","author":"Spitz","year":"1991","journal-title":"J. Dent. Res."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Men, X., Shibata, Y., Takeshita, T., and Yamashita, Y. (2016). Identification of Anion Channels Responsible for Fluoride Resistance in Oral Streptococci. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0165900"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Murata, T., and Hanada, N. (2016). Contribution of chloride channel permease to fluoride resistance in Streptococcus mutans. FEMS Microbiol. Lett., 363.","DOI":"10.1093\/femsle\/fnw101"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.archoralbio.2019.01.016","article-title":"Deletion of cas3 gene in Streptococcus mutans affects biofilm formation and increases fluoride sensitivity","volume":"99","author":"Tang","year":"2019","journal-title":"Arch. Oral Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1270","DOI":"10.1177\/0022034520927385","article-title":"Intrinsic Fluoride Tolerance Regulated by a Transcription Factor","volume":"99","author":"Lu","year":"2020","journal-title":"J. Dent. Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1111\/omi.12316","article-title":"Identification of Streptococcus mutans genes involved in fluoride resistance by screening of a transposon mutant library","volume":"35","author":"Yu","year":"2020","journal-title":"Mol. Oral Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1080\/08927014.2012.672646","article-title":"Enhancement of fluoride activity against Streptococcus mutans biofilms by a substance separated from Polygonum cuspidatum","volume":"28","author":"Pandit","year":"2012","journal-title":"Biofouling"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1159\/000534055","article-title":"Green Tea-Derived Catechins Suppress the Acid Productions of Streptococcus mutans and Enhance the Efficiency of Fluoride","volume":"57","author":"Han","year":"2023","journal-title":"Caries Res."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Liu, J., Weng, Q., Da, D., Yao, S., Zhang, Y., and Wu, Y. (2024). Enhancement of Fluoride\u2019s Antibacterial and Antibiofilm Effects against Oral Staphylococcus aureus by the Urea Derivative BPU. Antibiotics, 13.","DOI":"10.3390\/antibiotics13100930"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1177\/0022034514561259","article-title":"Combinatorial effects of arginine and fluoride on oral bacteria","volume":"94","author":"Zheng","year":"2015","journal-title":"J. Dent. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1016\/j.biotechadv.2008.08.001","article-title":"Non-thermal plasma technologies: New tools for bio-decontamination","volume":"26","author":"Moreau","year":"2008","journal-title":"Biotechnol. Adv."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1409","DOI":"10.1109\/TPS.2002.804220","article-title":"Nonthermal decontamination of biological media by atmospheric-pressure plasmas: Review, analysis, and prospects","volume":"30","author":"Laroussi","year":"2002","journal-title":"IEEE Trans. Plasma Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1257","DOI":"10.1109\/TPS.2006.878381","article-title":"Bactericidal Action of the Reactive Species Produced by Gas-Discharge Nonthermal Plasma at Atmospheric Pressure: A Review","volume":"34","author":"Gaunt","year":"2006","journal-title":"IEEE Trans. Plasma Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1120","DOI":"10.1002\/ppap.201400068","article-title":"Reactive Species from Cold Atmospheric Plasma: Implications for Cancer Therapy","volume":"11","author":"Graves","year":"2014","journal-title":"Plasma Process. Polym."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1002\/ppap.201400071","article-title":"Anti-Cancer Therapies of 21st Century: Novel Approach to Treat Human Cancers Using Cold Atmospheric Plasma","volume":"11","author":"Ratovitski","year":"2014","journal-title":"Plasma Process. Polym."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.procbio.2021.11.017","article-title":"Cold atmospheric plasma therapy in wound healing","volume":"112","author":"Dubey","year":"2022","journal-title":"Process Biochem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"477","DOI":"10.4062\/biomolther.2014.105","article-title":"Non-thermal atmospheric-pressure plasma possible application in wound healing","volume":"22","author":"Haertel","year":"2014","journal-title":"Biomol. Ther."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"36652","DOI":"10.1109\/ACCESS.2020.2971222","article-title":"Non-Thermal Bio-Compatible Plasma Induces Osteogenic Differentiation of Human Mesenchymal Stem\/Stromal Cells With ROS-Induced Activation of MAPK","volume":"8","author":"Li","year":"2020","journal-title":"IEEE Access"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Choi, B.-B., Choi, J.-H., Kang, T.-H., Lee, S.-J., and Kim, G.-C. (2021). Enhancement of Osteoblast Differentiation Using No-Ozone Cold Plasma on Human Periodontal Ligament Cells. Biomedicines, 9.","DOI":"10.3390\/biomedicines9111542"},{"key":"ref_43","first-page":"e58663","article-title":"Nerve Stem Cell Differentiation by a One-step Cold Atmospheric Plasma Treatment In Vitro","volume":"143","author":"Xiong","year":"2019","journal-title":"J. Vis. Exp."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1007\/s13346-020-00808-2","article-title":"Applications of cold atmospheric plasma for transdermal drug delivery: A review","volume":"11","author":"Wen","year":"2020","journal-title":"Drug Deliv. Transl. Res."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Hong, Q., Dong, X., Chen, M., Sun, H., Hong, L., Wang, Y., Li, H., and Yu, Q. (2019). An in vitro and in vivo study of plasma treatment effects on oral biofilms. J. Oral Microbiol., 11.","DOI":"10.1080\/20002297.2019.1603524"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1002\/ppap.200600077","article-title":"Bacterial Deactivation Using a Low Temperature Argon Atmospheric Plasma Brush with Oxygen Addition","volume":"4","author":"Huang","year":"2007","journal-title":"Plasma Process. Polym."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.jdent.2010.10.002","article-title":"Oral bacterial deactivation using a low-temperature atmospheric argon plasma brush","volume":"39","author":"Yang","year":"2011","journal-title":"J. Dent."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"07LG02","DOI":"10.7567\/JJAP.55.07LG02","article-title":"Disinfection of Streptococcus mutans biofilm by a non-thermal atmospheric plasma brush","volume":"55","author":"Hong","year":"2016","journal-title":"Jpn. J. Appl. Phys."},{"key":"ref_49","first-page":"84","article-title":"Plasma deactivation of oral bacteria seeded on hydroxyapatite disks as tooth enamel analogue","volume":"27","author":"Blumhagen","year":"2014","journal-title":"Am. J. Dent."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2910","DOI":"10.1109\/TPS.2022.3196226","article-title":"Effects of Atmospheric Fluorine-Containing Nonthermal Plasmas on Demineralization and Remineralization of Tooth Enamel","volume":"50","author":"Dong","year":"2022","journal-title":"IEEE Trans. Plasma Sci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1111\/j.1600-0722.2010.00761.x","article-title":"Dentin surface treatment using a non-thermal argon plasma brush for interfacial bonding improvement in composite restoration","volume":"118","author":"Ritts","year":"2010","journal-title":"Eur. J. Oral Sci."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Hong, Q., Sun, H., Chen, M., Zhang, S., and Yu, Q. (2022). Plasma treatment effects on destruction and recovery of Porphyromonas gingivalis biofilms. PLoS ONE, 17.","DOI":"10.1371\/journal.pone.0274523"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2945","DOI":"10.1002\/elps.201300206","article-title":"Enhanced penetration of fluoride particles into bovine enamel by combining dielectrophoresis with AC electroosmosis","volume":"34","author":"Ivanoff","year":"2013","journal-title":"Electrophoresis"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1177\/0022034518818463","article-title":"Enhanced Delivery of F(-), Ca(2+), K(+), and Na(+) Ions into Enamel by Electrokinetic Flows","volume":"98","author":"Peng","year":"2019","journal-title":"J. Dent. Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1002\/jbm.b.30586","article-title":"Bacterial inactivation using a low-temperature atmospheric plasma brush sustained with argon gas","volume":"80","author":"Yu","year":"2007","journal-title":"J. Biomed. Mater. Res. B Appl. Biomater."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1007\/s00248-020-01531-8","article-title":"Shifts in Composition and Activity of Oral Biofilms After Fluoride Exposure","volume":"80","author":"Mira","year":"2020","journal-title":"Microb. Ecol."}],"container-title":["Journal of Functional Biomaterials"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-4983\/16\/4\/132\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:10:36Z","timestamp":1760029836000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-4983\/16\/4\/132"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,4,5]]},"references-count":56,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2025,4]]}},"alternative-id":["jfb16040132"],"URL":"https:\/\/doi.org\/10.3390\/jfb16040132","relation":{},"ISSN":["2079-4983"],"issn-type":[{"value":"2079-4983","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,4,5]]}}}