JIOH on LinkedIn JIOH on Facebook
  • Users Online: 178
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Ahead of print Current issue Search Archives Submit article Instructions Subscribe Contacts Login 

 Table of Contents  
Year : 2021  |  Volume : 13  |  Issue : 4  |  Page : 326-330

The role of cold atmospheric plasma (CAP) in the control of biofilms on titanium surfaces: A Literature review

1 Academic Department, Faculty of Dentistry, Universidad Nacional Federico Villarreal, Lima, Peru
2 PhD Department, Faculty of Dentistry, Universidad Nacional Federico Villarreal, Lima, Peru
3 Postgraduate Department, CHANGE Research Working Group, Faculty of Health Sciences, Universidad Científica del Sur, Lima, Peru

Date of Submission24-Jan-2021
Date of Decision02-Apr-2021
Date of Acceptance15-May-2021
Date of Web Publication19-Aug-2021

Correspondence Address:
Dr. Frank Mayta-Tovalino
Postgraduate Department, Faculty of Health of Sciences, Universidad Científica del Sur, Lima.
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/JIOH.JIOH_17_21

Rights and Permissions

Aim: Cold atmospheric plasma (CAP) is frequently used for the sterilization of biomaterials in the field of dentistry. The aim of this narrative review is to present the role of CAP in the control of biofilms on titanium surfaces. Materials and Methods: The PubMed, Scopus, and WOS databases were searched to identify scientific articles published between 2010 and 2020, with the keywords “biofilm,” “cold atmospheric temperature,” and “titanium,” using the logical operators AND and OR. Results: We found 8 articles in PubMed, 11 in Scopus, and 10 in WOS, including review articles and original studies, among others. All the articles were selected by two independent reviewers according to the eligibility criteria. Conclusions: Despite the restrictions of this review, CAP seems to have an effect on titanium surfaces in the oral area. Studies have shown that bacterial biofilms become inactive after 3 min of plasma treatment.

Keywords: Biofilm, Cold Atmospheric Plasma, Titanium Surfaces

How to cite this article:
Garcia L, Rojas L, Gonzales G, Alvitez-Temoche D, Mendoza R, Mayta-Tovalino F. The role of cold atmospheric plasma (CAP) in the control of biofilms on titanium surfaces: A Literature review. J Int Oral Health 2021;13:326-30

How to cite this URL:
Garcia L, Rojas L, Gonzales G, Alvitez-Temoche D, Mendoza R, Mayta-Tovalino F. The role of cold atmospheric plasma (CAP) in the control of biofilms on titanium surfaces: A Literature review. J Int Oral Health [serial online] 2021 [cited 2021 Oct 26];13:326-30. Available from:

  Introduction Top

The CAP is attracting great interest from scientists as possible therapies in dentistry and other areas of medicine.[1],[2] Plasma technology is a novel procedure with good prospects; it is an efficient method at low temperatures and does not leave associated chemical residues. The CAP has been shown to be effective against many pathogens, including prions and bacterial spores, which exhibit high-level resistance to physical and chemical treatments.[3]

Plasma is considered the fourth state of matter (after the gaseous, liquid, and solid forms),[4] and it was discovered by William Crookes in 1879.[5] Further, it can be classified as low- and high-temperature plasma, also called thermal and nonthermal plasma, respectively.[6] Despite the presence of high-temperature electrons and ions, nonthermal plasma remains stable at room temperature; this is why it is known as CAP.[7] This characteristic makes CAP suitable for various applications in the health sciences.[8]

The CAP comprised ionized gases formed by charged particles in which a reactive mixture is produced when interacting with the surrounding air,[9] generally causing them to have a temperature close to room temperature.[10],[11] The CAP contains various biologically active species, including oxygen and nitrogen particles,.[12] photons, ultraviolet ions, and electrons.[13],[14],[15] The use of plasma at atmospheric pressure can help overcome the disadvantages of vacuum systems and induces physical and chemical changes in biological materials[16],[17] without causing thermal or electrical damage to the cell surface of healthy tissues.[18],[19]

The aim of this literature review is to present the role of CAP in controlling the formation of biofilms on titanium surfaces.

  Materials and Methods Top

For this narrative review, the PubMed, Scopus, and Web of Science databases were searched to identify scientific articles published between January 2010 and December 2020, with the keywords “biofilm,” “cold atmospheric plasma,” and “dental implant,” for which the logical operators AND and OR were used. Data extraction was carried out according to the PICO strategy:

  • P: Patients with dental implant

  • I: Application of cold atmospheric plasma

  • C: Other care protocols

  • O: Destruction of oral biofilm

Search strategy

The following search strategy was used:

(“biofilm s”[All Fields] OR “biofilmed”[All Fields] OR “biofilms”[MeSH Terms] OR “biofilms”[All Fields] OR “biofilm”[All Fields]) AND ((“common cold”[MeSH Terms] OR (“common”[All Fields] AND “cold”[All Fields]) OR “common cold”[All Fields] OR “cold”[All Fields] OR “cold temperature”[MeSH Terms] OR (“cold”[All Fields] AND “temperature”[All Fields]) OR “cold temperature”[All Fields]) AND (“atmosphere”[MeSH Terms] OR “atmosphere”[All Fields] OR “atmospheres”[All Fields] OR “atmospheric”[All Fields] OR “atmospherical”[All Fields] OR “atmospherically”[All Fields] OR “atmospherics”[All Fields]) AND (“plasma”[MeSH Terms] OR “plasma”[All Fields] OR “plasmas”[All Fields] OR “plasma s”[All Fields])) AND (“titanium”[MeSH Terms] OR “Dental implant”[All Fields] OR “titaniums”[All Fields])

The search yielded 8 articles in PubMed, 11 in Scopus, and 10 in WOS, including review articles and original studies, among others. All the articles were selected by two independent reviewers according to the eligibility criteria.

Selection criteria

Experimental, epidemiological, and descriptive studies on biofilms, cold atmospheric temperature, and titanium

  • Manuscripts that explain the role of CAP

  • Manuscripts published between 2010 and 2020

  • Manuscripts in all languages

Risk of bias

Since this is a narrative review, there is potential for risk of bias; this is explained when discussing the limitations of this review.

  Results Top

Applications of CAP in medicine

The CAP has been shown to control microbial load without negative effects on healthy tissues; therefore, its use to reduce bacterial content should be indicated. The CAP has also been shown to have tissue regeneration, anti-inflammatory, and antitumor effects, and it can decontaminate biotic and abiotic surfaces.[20],[21],[22] Moreover, it acts on stem cells and other cultured cells, and even at very high levels of nitric oxide, has an important effect on their proliferation [Table 1].[22]
Table 1: Studies on the use of CAP

Click here to view

Applications of CAP in dentistry

In the field of oral medicine, CAP has been used in the treatment of certain oral diseases such as dental caries, peri-implantitis, periodontal disease, and endodontic infections.[23] It has been shown that CAP has the potential to inactivate biofilms of S. mutans, which is the main causal organism of dental caries.[2] An additional advantage of CAP is its relative ease of application on uneven surface sites in the oral cavity. Sufficiently miniature device discharge can also be employed directly in the dental canal.[16] The CAP has been applied in the field of endodontics as well; some in vitro studies showed that CAP was significantly better at reducing Enterococcus faecalis loads than chemical irrigation with Clorhexidine at 0.1% and NaOCl at 0.6%. The objective of treatment of the root canal is to remove all bacteria that are in the root canal system and prevent reinfection.[23],[24]


Some researchers have demonstrated that the amount of biofilms on titanium disks that were treated with CAP was lower than that on disks subjected to other treatments; however, it was not possible to eliminate the biofilms.[25],[26] The CAP affects titanium in the mouth by modifying the hydrophilicity and irregularities of this metal. Both these factors have a positive effect on the proliferation, cellular union, and maturation of osteoblasts, and they may facilitate accelerated osseointegration. Although the increase in roughness due to the application of CAP can lead to a greater accumulation of bacteria, its antimicrobial capacity can minimize this negative results. These findings suggest that CAP-based mechanisms are appropriate for the treatment of peri-implant inflammation.[27]

  Discussion Top

Currently, the application of CAP is a promising technique for removing organic material from surfaces without causing damage to the underlying surface and producing toxic waste effects. The literature used for this review was a maximum of five years old, and mostly in vitro experimental research was used. Experimental in vivo investigations using CAP are generally studies on osseointegration and were, therefore, not considered for this review article. Biofilms found in implants induce the inflammation of the soft tissues adjacent to the implant, and they lead to failures in surgery and placement of the implant because of peri-implantitis caused by the organisms in the biofilms.[27]

This narrative review focused mainly on the elimination of bacterial biofilms on the surfaces of implants; however, some considerations were made since both the design of the implant and the rough texture of the surface prevent the elimination of biofilms. An investigation by Duske et al. showed that a clean surface was obtained in front of a bacterial plaque owing to the combination of brushing treatments and subsequent CAP treatment, which paved the way for cell growth, similar to that observed with sterile control cells. Hence, the combination of brushing and CAP treatment is an effective option for the disinfection of titanium implants.[27] Matthes et al. investigated whether biofilms could be removed by a combination of optimized air (AP) and cold in vitro cell plasma (CAP) in 200 titanium disk samples. The AP procedure was defined as having the potential to reduce oral biofilm content from surfaces in the entirety of the implant; however, AP + CAP treatment did not produce results as good as those of biofilm removal using solitary AP treatment.[28]

Streptococcus mitis is found in oral flora, and although it acts as an opportunist, it is a precursor in the formation of a biofilm and helps the coadherence of colonizers at the beginning of the biofilm formation process. The antibacterial efficacy of CAP has been widely tested, and it is known that it has nothing to do with the distribution of the plasma, since plasma spreads over surfaces and even penetrates porous structures. Preissner et al. conducted a study comparing the efficacy of plasma, a diode laser, and 1% NaC against S. mitis; the number of dead cells obtained in the plasma treatment was higher than that obtained using the laser and NaC.[29],[30] Canullo et al. carried out a study with 720 titanium disks contaminated with S. mitis; they observed that after 60 s of treatment with argon, the adhesion of bacteria significantly reduced. They concluded that the implant surface was disinfected.[31]

Among the studies on biofilms and their elimination, in 2016, Ibis et al.[30] investigated the formation of Escherichia coli and Staphylococcus aureus biofilms and showed that 95% of both microorganisms were removed after a few minutes of the plasma procedure. Based on their study of S. aureus, Ulu et al. concluded that the application of plasma on the surface of a titanium disk for 120 s reduced approximately 62% of the mass of the biofilm obtained; its roughness did not change significantly and its temperature (30–33°C) did not increase to dangerous limits (31.6°C), which may have caused necrosis.

Porphyromonas gingivalis is a pathogen that facilitates periodontitis and re-perimplantitis. The results of in vitro studies on P. gingivalis by Lee et al. showed that CAP was effective in decontaminating biofilms on SLA surfaces without surface alterations, and CAP also eliminated bacteria from sites exposed to plasma directly as well as those that were unexposed. Recently, Yang et al. showed that hydrophilicity and surface roughness improved after CAP treatment, which completely eliminated P. gingivalis.[11],[32],[33]

This review has some limitations. One is the lack of homogenization in various aspects related to the methodology. In the contamination methodology, diverse pathogens were employed, with the most prevalent being P. gingivalis. Moreover, different configurations of time and power used by various authors were evaluated in this study. Another limitation was the restricted accessibility to diverse magazines that contain updated articles on CAP. In addition, studies on the removal of bacterial plaque on the surface of implants have not been performed. However, the strengths of this review are that updated CAP research papers were referred, and scientific evidence indicates that the use of CAP favors biofilm removal on titanium surfaces.

  Conclusions Top

The CAP has a significant effect on titanium structures in the oral cavity. Studies have shown that bacterial biofilms become inactive after 3 min of plasma treatment. Such treatments eliminate bacteria from sites directly exposed to the plasma, as well as those not exposed to it, and even improve hydrophilicity and surface roughness. Hence, the use of CAP may be a good strategy for the decontamination of titanium surfaces.


The authors would like to thank the Universidad Cientifica del Sur for supporting the preparation of this article.

Financial support and sponsorship

None to declare.

Conflicts of interest

There are no personal interests to declare.

Authors’ contributions

LG, LR, and GG: concept and design of study, drafting, and revision. FMT, RM, and DAT: acquisition of data, analysis, and interpretation. FMT, DAT, and RM: acquisition of data, interpretation, and drafting. Finally, all authors had given approval of the version of the article to be published.

Ethical policy and Institutional Review board statement

Not applicable.

Patient declaration of consent

Not applicable.

Data availability statement

Within this article, the presented data set was retrieved from original articles. The data are already present in these articles.

  References Top

Niedźwiedź I, Waśko A, Pawłat J, Polak-Berecka M. The state of research on antimicrobial activity of cold plasma. Pol J Microbiol 2019;68:153-64.  Back to cited text no. 1
Hoffmann C, Berganza C, Zhang J. Cold atmospheric plasma: Methods of production and application in dentistry and oncology. Med Gas Res 2013;3:21.  Back to cited text no. 2
Sakudo A, Yagyu Y, Onodera T. Disinfection and sterilization using plasma technology: Fundamentals and future perspectives for biological applications. Int J Mol Sci 2019;20:5216.  Back to cited text no. 3
Jha N, Ryu JJ, Wahab R, Al-Khedhairy AA, Choi EH, Kaushik NK. Treatment of oral hyperpigmentation and gummy smile using lasers and role of plasma as a novel treatment technique in dentistry: An introductory review. Oncotarget 2017;8:20496-509.  Back to cited text no. 4
Arora V, Nikhil V, Suri NK, Arora P. Cold atmospheric plasma (CAP) in dentistry. Dentistry 2014;4:189.  Back to cited text no. 5
Ranjan R, Krishnamraju PV, Shankar T, Gowd S. Nonthermal plasma in dentistry: An update. J Int Soc Prev Community Dent 2017;7:71-5.  Back to cited text no. 6
Farasat M, Arjmand S, Ranaei Siadat SO, Sefidbakht Y, Ghomi H. The effect of non-thermal atmospheric plasma on the production and activity of recombinant phytase enzyme. Sci Rep 2018;8:16647.  Back to cited text no. 7
Rezaeinezhad A, Eslami P, Mirmiranpour H, Ghomi H. The effect of cold atmospheric plasma on diabetes-induced enzyme glycation, oxidative stress, and inflammation; in vitro and in vivo. Sci Rep 2019;9:19958.  Back to cited text no. 8
Theinkom F, Singer L, Cieplik F, Cantzler S, Weilemann H, Cantzler M, et al. Antibacterial efficacy of cold atmospheric plasma against Enterococcus faecalis planktonic cultures and biofilms in vitro. PLoS One 2019;14:e0223925.  Back to cited text no. 9
Gherardi M, Tonini R, Colombo V. Plasma in dentistry: Brief history and current status. Trends Biotechnol 2018;36:583-5.  Back to cited text no. 10
Rao Y, Shang W, Yang Y, Zhou R, Rao X. Fighting mixed-species microbial biofilms with cold atmospheric plasma. Front Microbiol 2020;11:1000.  Back to cited text no. 11
Haralambiev L, Wien L, Gelbrich N, Lange J, Bakir S, Kramer A, et al. Cold atmospheric plasma inhibits the growth of osteosarcoma cells by inducing apoptosis, independent of the device used. Oncol Lett 2020;19:283-90.  Back to cited text no. 12
de Groot GJJB, Hundt A, Murphy AB, Bange MP, Mai-Prochnow A. Cold plasma treatment for cotton seed germination improvement. Sci Rep 2018;8:14372.  Back to cited text no. 13
Scharf C, Eymann C, Emicke P, Bernhardt J, Wilhelm M, Görries F, et al. Improved wound healing of airway epithelial cells is mediated by cold atmospheric plasma: A time course-related proteome analysis. Oxid Med Cell Longev 2019;2019:7071536.  Back to cited text no. 14
Tan F, Fang Y, Zhu L, Al-Rubeai M. Controlling stem cell fate using cold atmospheric plasma. Stem Cell Res Ther 2020;11:368.  Back to cited text no. 15
Hojnik N, Cvelbar U, Tavčar-Kalcher G, Walsh JL, Križaj I. Mycotoxin decontamination of food: Cold atmospheric pressure plasma versus “Classic” decontamination. Toxins (Basel) 2017;9:151.  Back to cited text no. 16
Gay-Mimbrera J, García MC, Isla-Tejera B, Rodero-Serrano A, García-Nieto AV, Ruano J. Clinical and biological principles of cold atmospheric plasma application in skin cancer. Adv Ther 2016;33:894-909.  Back to cited text no. 17
Keidar M, Walk R, Shashurin A, Srinivasan P, Sandler A, Dasgupta S, et al. Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. Br J Cancer 2011;105:1295-301.  Back to cited text no. 18
Adhikari B, Pangomm K, Veerana M, Mitra S, Park G. Plant disease control by non-thermal atmospheric-pressure plasma. Front Plant Sci 2020;11:77.  Back to cited text no. 19
Bernhardt T, Semmler ML, Schäfer M, Bekeschus S, Emmert S, Boeckmann L. Plasma medicine: Applications of cold atmospheric pressure plasma in dermatology. Oxid Med Cell Longev 2019;2019:3873928.  Back to cited text no. 20
Connor M, Flynn PB, Fairley DJ, Marks N, Manesiotis P, Graham WG, et al. Evolutionary clade affects resistance of clostridium difficile spores to cold atmospheric plasma. Sci Rep 2017;7:41814.  Back to cited text no. 21
Braný D, Dvorská D, Halašová E, Škovierová H. Cold atmospheric plasma: A powerful tool for modern medicine. Int J Mol Sci 2020;21:2932.  Back to cited text no. 22
Hui WL, Perrotti V, Iaculli F, Piattelli A, Quaranta A. The emerging role of cold atmospheric pilasma in implantology: A review of the literature. Nanomaterials (Basel) 2020;10:1505.  Back to cited text no. 23
Jiao Y, Tay FR, Niu LN, Chen JH. Advancing antimicrobial strategies for managing oral biofilm infections. Int J Oral Sci 2019;11:28.  Back to cited text no. 24
Rupf S, Idlibi AN, Umanskaya N, Hannig M, Nothdurft F, Lehmann A, et al. Disinfection and removal of biofilms on microstructured titanium by cold atmospheric plasma. Deutscher Ärzte-Verlag 2012;3:126-37.  Back to cited text no. 25
Idlibi AN, Al-Marrawi F, Hannig M, Lehmann A, Rueppell A, Schindler A, et al. Destruction of oral biofilms formed in situ on machined titanium (Ti) surfaces by cold atmospheric plasma. Biofouling 2013;29:369-79.  Back to cited text no. 26
Duske K, Jablonowski L, Koban I, Matthes R, Holtfreter B, Sckell A, et al. Cold atmospheric plasma in combination with mechanical treatment improves osteoblast growth on biofilm covered titanium discs. Biomaterials 2015;52:327-34.  Back to cited text no. 27
Matthes R, Duske K, Kebede TG, Pink C, Schlüter R, von Woedtke T, et al. Osteoblast growth, after cleaning of biofilm-covered titanium discs with air-polishing and cold plasma. J Clin Periodontol 2017;44:672-80.  Back to cited text no. 28
Preissner S, Wirtz HC, Tietz AK, Abu-Sirhan S, Herbst SR, Hartwig S, et al. Bactericidal efficacy of tissue tolerable plasma on microrough titanium dental implants: An in-vitro-study. J Biophotonics 2016;9:637-44.  Back to cited text no. 29
Ibis F, Oflaz H, Ercan UK. Biofilm inactivation and prevention on common implant material surfaces by nonthermal DBD plasma treatment. Plasma Med 2016;6:33-45.  Back to cited text no. 30
Canullo L, Genova T, Wang HL, Carossa S, Mussano F. Plasma of argon increases cell attachment and bacterial decontamination on different implant surfaces. Int J Oral Maxillofac Implants 2017;32:1315-23.  Back to cited text no. 31
Ulu M, Pekbagriyanik T, Ibis F, Enhos S, Ercan UK. Antibiofilm efficacies of cold plasma and er: YAG laser on staphylococcus aureus biofilm on titanium for nonsurgical treatment of peri-implantitis. Niger J Clin Pract 2018;21:758-65.  Back to cited text no. 32
[PUBMED]  [Full text]  
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.  Back to cited text no. 33


  [Table 1]


Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  In this article
Materials and Me...
Article Tables

 Article Access Statistics
    PDF Downloaded35    
    Comments [Add]    

Recommend this journal