Top

Clinical Oral Investigations

Published in:

01-04-2020 | Original Article

Inhibition of bacterial growth on zirconia abutment with a helium cold atmospheric plasma jet treatment

Authors: Yang Yang, Miao Zheng, Yang Yang, Jing Li, Yong-Fei Su, He-Ping Li, Jian-Guo Tan

Published in: Clinical Oral Investigations | Issue 4/2020

Abstract

Objectives

This study presents a surface modification method to treat the zirconia implant abutment materials using a helium cold atmospheric plasma (CAP) jet in order to evaluate its efficacy on oral bacteria adhesion and growth.

Materials and methods

Yttrium-Stabilized Zirconia disks were subjected to helium CAP treatment; after the treatment, zirconia surface was evaluated using scanning electron microscopy, a contact angle measuring device, X-ray photoelectron spectroscopy for surface characteristics. The response of Streptococcus mutans and Porphyromonas gingivalis on treated surface was evaluated by a scanning electron microscopy, MTT assay, and LIVE/DEAD staining. The biofilm formation was analyzed using a crystal violet assay.

Results

After the helium CAP jet treatment, the zirconia surface chemistry has been changed while the surface topography remains unchanged, the bacterial growth was inhibited, and the biofilm forming decreased. As the treatment time increases, the zirconia abutment showed a better bacterial inhibition efficacy.

Conclusions

The helium CAP jet surface modification approach can eliminate bacterial growth on zirconia surface with surface chemistry change, while surface topography remained.

Clinical relevance

Soft tissue seal around dental implant abutment plays a crucial role in maintaining long-term success. However, it is weaker than periodontal barriers and vulnerable to bacterial invasion. CAP has a potential prospect for improving soft tissue seal around the zirconia abutment, therefore providing better esthetics and most of all, prevent peri-implant lesions from happening.

Berglundh T, Lindhe J, Ericsson I, Marinello CP, Liljenberg B, Thomsen P (1991) The soft tissue barrier at implants and teeth. Clin Oral Implants Res 2:81–90. https://doi.org/10.1034/j.1600-0501.1991.020206.x CrossRefPubMed

Ivanovski S, Lee R (2018) comparison of peri-implant and periodontal marginal soft tissues in health and disease. Periodontol 2000 76:116–130. https://doi.org/10.1111/prd.12150

Renvert S, Quirynen M (2015) Risk indicators for peri-implantitis. A narrative review. Clin Oral Implants Res 26:15–44. https://doi.org/10.1111/clr.12636 CrossRefPubMed

Rakic M, Galindo-Moreno P, Monje A, Radovanovic S, Wang H-L, Cochran D, Sculean A, Canullo L (2017) How frequent does peri-implantitis occur? A systematic review and meta-analysis. Clin Oral Investig 22:1805–1816. https://doi.org/10.1007/s00784-017-2276-y CrossRefPubMed

Wang Y, Zhang Y, Miron RJ (2016) Health, maintenance, and recovery of soft tissues around implants. Clin Implant Dent R 18:618–634. https://doi.org/10.1111/cid.12343 CrossRef

Salvi GE, Bosshardt DD, Lang NP, Abrahamsson I, Berglundh T, Lindhe J, Ivanovski S, Donos N (2015) Temporal sequence of hard and soft tissue healing around titanium dental implants. Periodontol 68:135–152. https://doi.org/10.1111/prd.12054 CrossRef

Gristina A (1987) Biomaterial-centered infection: microbial adhesion versus tissue integration. Science 237:1588–1595. https://doi.org/10.1126/science.3629258 CrossRefPubMed

Fürst MM, Salvi GE, Lang NP, Persson GR (2007) Bacterial colonization immediately after installation on oral titanium implants. Clin Oral Implants Res 18:501–508. https://doi.org/10.1111/j.1600-0501.2007.01381.x CrossRefPubMed

Subbiahdoss G, Grijpma DW, van der Mei HC, Busscher HJ, Kuijer R (2010) Microbial biofilm growth versus tissue integration on biomaterials with different wettabilities and a polymer-brush coating. J Biomed Mater Res A 94:533–538. https://doi.org/10.1002/jbm.a.32731 CrossRefPubMed

10.

Sculean A, Gruber R, Bosshardt DD (2014) Soft tissue wound healing around teeth and dental implants. J Clin Periodontol 41:S6–S22. https://doi.org/10.1111/jcpe.12206 CrossRefPubMed

11.

Tomasi C, Tessarolo F, Caola I, Piccoli F, Wennström JL, Nollo G, Berglundh T (2016) Early healing of peri-implant mucosa in man. J Clin Periodontol 43:816–824. https://doi.org/10.1111/jcpe.12591 CrossRefPubMed

12.

Han A, Tsoi JKH, Rodrigues FP, Leprince JG, Palin WM (2016) Bacterial adhesion mechanisms on dental implant surfaces and the influencing factors. Int J Adhes Adhes 69:58–71. https://doi.org/10.1016/j.ijadhadh.2016.03.022 CrossRef

13.

Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144. https://doi.org/10.1111/j.1600-051X.1998.tb02419.x CrossRefPubMed

14.

Werner S, Huck O, Frisch B, Vautier D, Elkaim R, Voegel J-C, Brunel G, Tenenbaum H (2009) The effect of microstructured surfaces and laminin-derived peptide coatings on soft tissue interactions with titanium dental implants. Biomaterials 30:2291–2301. https://doi.org/10.1016/j.biomaterials.2009.01.004 CrossRefPubMed

15.

Teughels W, Van Assche N, Sliepen I, Quirynen M (2006) Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res 17:68–81. https://doi.org/10.1111/j.1600-0501.2006.01353.x CrossRefPubMed

16.

Larsson A, Andersson M, Wigren S, Pivodic A, Flynn M, Nannmark U (2015) Soft tissue integration of hydroxyapatite-coated abutments for bone conduction implants. Clin Implant Dent R 17:e730–e735. https://doi.org/10.1111/cid.12304 CrossRef

17.

Sanz-Martín I, Sanz-Sánchez I, Carrillo de Albornoz A, Figuero E, Sanz M (2018) Effects of modified abutment characteristics on peri-implant soft tissue health: a systematic review and meta-analysis. Clin Oral Implants Res 29:118–129. https://doi.org/10.1111/clr.13097 CrossRefPubMed

18.

Fretwurst T, Nelson K, Tarnow DP, Wang HL, Giannobile WV (2018) Is metal particle release associated with peri-implant bone destruction? An emerging concept. J Dent Res 97:259–265. https://doi.org/10.1177/0022034517740560 CrossRefPubMed

19.

Lorenz J, Giulini N, Hölscher W, Schwiertz A, Schwarz F, Sader R (2019) Prospective controlled clinical study investigating long-term clinical parameters, patient satisfaction, and microbial contamination of zirconia implants. Clin Implant Dent R 21:263–271. https://doi.org/10.1111/cid.12720 CrossRef

20.

Blatz MB, Bergler M, Holst S, Block MS (2009) Zirconia abutments for single-tooth implants—rationale and clinical guidelines. J Oral Maxillofac Surg 67:74–81. https://doi.org/10.1016/j.joms.2009.07.011 CrossRefPubMed

21.

Al-Radha ASD, Dymock D, Younes C, O'Sullivan D (2012) Surface properties of titanium and zirconia dental implant materials and their effect on bacterial adhesion. J Dent 40:146–153. https://doi.org/10.1016/j.jdent.2011.12.006 CrossRefPubMed

22.

Hashim D, Cionca N, Courvoisier DS, Mombelli A (2016) A systematic review of the clinical survival of zirconia implants. Clin Oral Investig 20:1403–1417. https://doi.org/10.1007/s00784-016-1853-9 CrossRefPubMedPubMedCentral

23.

Yang Y, Zhou J, Liu X, Zheng M, Yang J, Tan J (2015) Ultraviolet light-treated zirconia with different roughness affects function of human gingival fibroblastsin vitro: the potential surface modification developed from implant to abutment. J Biomed Mater Res B 103:116–124. https://doi.org/10.1002/jbm.b.33183 CrossRef

24.

Liu M, Zhou J, Yang Y, Zheng M, Yang J, Tan J (2015) Surface modification of zirconia with polydopamine to enhance fibroblast response and decrease bacterial activity in vitro : a potential technique for soft tissue engineering applications. Colloids Surf B: Biointerfaces 136:74–83. https://doi.org/10.1016/j.colsurfb.2015.06.047 CrossRefPubMed

25.

Abdallah M-N, Badran Z, Ciobanu O, Hamdan N, Tamimi F (2017) Strategies for optimizing the soft tissue seal around osseointegrated implants. Adv Healthc Mater:6. https://doi.org/10.1002/adhm.201700549

26.

Li H-P, Zhang X-F, Zhu X-M, Zheng M, Liu S-F, Qi X, Wang K-P, Chen J, Xi X-Q, Tan J-G, Ostrikov K (2017) Translational plasma stomatology: applications of cold atmospheric plasmas in dentistry and their extension. High Voltage 2:188–199. https://doi.org/10.1049/hve.2017.0066 CrossRef

27.

Garcia B, Camacho F, Peñarrocha D, Tallarico M, Perez S, Canullo L (2017) Influence of plasma cleaning procedure on the interaction between soft tissue and abutments: a randomized controlled histologic study. Clin Oral Implants Res 28:1269–1277. https://doi.org/10.1111/clr.12953 CrossRefPubMed

28.

Canullo L, Tallarico M, Botticelli D, Alccayhuaman KAA, Martins Neto EC, Xavier SP (2018) Hard and soft tissue changes around implants activated using plasma of argon: a histomorphometric study in dog. Clin Oral Implants Res 29:389–395. https://doi.org/10.1111/clr.13134 CrossRefPubMed

29.

Canullo L, Peñarrocha D, Clementini M, Iannello G, Micarelli C (2015) Impact of plasma of argon cleaning treatment on implant abutments in patients with a history of periodontal disease and thin biotype: radiographic results at 24-month follow-up of a RCT. Clin Oral Implants Res 26:8–14. https://doi.org/10.1111/clr.12290 CrossRefPubMed

30.

Liao X, Liu D, Xiang Q, Ahn J, Chen S, Ye X, Ding T (2017) Inactivation mechanisms of non-thermal plasma on microbes: a review. Food Control 75:83–91. https://doi.org/10.1016/j.foodcont.2016.12.021 CrossRef

31.

Lunov O, Zablotskii V, Churpita O, Jäger A, Polívka L, Syková E, Dejneka A, Kubinová Š (2016) The interplay between biological and physical scenarios of bacterial death induced by non-thermal plasma. Biomaterials 82:71–83. https://doi.org/10.1016/j.biomaterials.2015.12.027 CrossRefPubMed

32.

Gilmore BF, Flynn PB, O’Brien S, Hickok N, Freeman T, Bourke P (2018) Cold plasmas for biofilm control: opportunities and challenges. Trends Biotechnol 36:627–638. https://doi.org/10.1016/j.tibtech.2018.03.007 CrossRefPubMed

33.

Lee JH, Jeong WS, Seo SJ, Kim HW, Kim KN, Choi EH, Kim KM (2017) Non-thermal atmospheric pressure plasma functionalized dental implant for enhancement of bacterial resistance and osseointegration. Dent Mater 33:257–270. https://doi.org/10.1016/j.dental.2016.11.011 CrossRefPubMed

34.

Canullo L, Genova T, Wang HL, Carossa S, Mussano F (2017) Plasma of argon increases cell attachment and bacterial decontamination on different implant surfaces. Int J Oral Maxillofac Implants 32:1315–1323. https://doi.org/10.11607/jomi.5777 CrossRefPubMed

35.

Genova T, Pesce P, Mussano F, Tanaka K, Canullo L (2019) The influence of bone-graft bio-functionalization with plasma of argon on bacterial contamination. J Biomed Mater Res A 107:67–70. https://doi.org/10.1002/jbm.a.36531 CrossRefPubMed

36.

Pistilli R, Genova T, Canullo L, Faga MG, Terlizzi ME, Gribaudo G, Mussano F (2018) Effect of bioactivation on traditional surfaces and zirconium nitride: adhesion and proliferation of preosteoblastic cells and bacteria. Int J Oral Maxillofac Implants 33:1247–1254. https://doi.org/10.11607/jomi.6654 CrossRefPubMed

37.

Lee MJ, Kwon JS, Jiang HB, Choi EH, Park G, Kim KM (2019) The antibacterial effect of non-thermal atmospheric pressure plasma treatment of titanium surfaces according to the bacterial wall structure. Sci Rep 9:1938. https://doi.org/10.1038/s41598-019-39414-9 CrossRefPubMedPubMedCentral

38.

Canullo L, Genova T, Tallarico M, Gautier G, Mussano F, Botticelli D (2016) Plasma of argon affects the earliest biological response of different implant surfaces: an in vitro comparative study. J Dent Res 95:566–573. https://doi.org/10.1177/0022034516629119 CrossRefPubMed

39.

Henningsen A, Smeets R, Hartjen P, Heinrich O, Heuberger R, Heiland M, Precht C, Cacaci C (2018) Photofunctionalization and non-thermal plasma activation of titanium surfaces. Clin Oral Investig 22:1045–1054. https://doi.org/10.1007/s00784-017-2186-z CrossRefPubMed

40.

Zheng M, Yang Y, Liu XQ, Liu MY, Zhang XF, Wang X, Li HP, Tan JG (2015) Enhanced biological behavior of in vitro human gingival fibroblasts on cold plasma-treated zirconia. PLoS One 10:e0140278. https://doi.org/10.1371/journal.pone.0140278 CrossRefPubMedPubMedCentral

41.

Li D, Li G, Li J, Liu Z-Q, Zhang X, Zhang Y, Li H-P (2019) Promotion of wound healing of genetic diabetic mice treated by a cold atmospheric plasma jet. IEEE T Plasma Sci 47:4848–4860. https://doi.org/10.1109/tps.2019.2928320

42.

Wu T, Hu W, Guo L, Finnegan M, Bradshaw DJ, Webster P, Loewy ZG, Zhou X, Shi W, Lux R (2013) Development of a new model system to study microbial colonization on dentures. J Prosthodont 22:344–350. https://doi.org/10.1111/jopr.12002 CrossRefPubMed

43.

Wang G, Feng H, Hu L, Jin W, Hao Q, Gao A, Peng X, Li W, Wong K-Y, Wang H, Li Z, Chu PK (2018) An antibacterial platform based on capacitive carbon-doped TiO2 nanotubes after direct or alternating current charging. Nat Commun 9:2055. https://doi.org/10.1038/s41467-018-04317-2 CrossRefPubMedPubMedCentral

44.

Li J, Guo H, Zhang X-F, Li H-P (2018) Numerical and experimental studies on the interactions between the radio-frequency glow discharge plasma jet and the shielding gas at atmosphere. IEEE Trans Plasma Sci 46:2766–2775. https://doi.org/10.1109/tps.2018.2852945 CrossRef

45.

Calliess T, Bartsch I, Haupt M, Reebmann M, Schwarze M, Stiesch M, Pfaffenroth C, Sluszniak M, Dempwolf W, Menzel H, Witte F, Willbold E (2016) In vivo comparative study of tissue reaction to bare and antimicrobial polymer coated transcutaneous implants. Mater Sci Eng C 61:712–719. https://doi.org/10.1016/j.msec.2015.12.095 CrossRef

46.

Quirynen M, Bollen CM (1995) The influence of surface roughness and surface-free energy on supra- and subgingival plaque formation in man. A review of the literature. J Clin Periodontol 22:1–14. https://doi.org/10.1111/j.1600-051X.1995.tb01765.x CrossRefPubMed

47.

Uyen M (1985) Surface free energies of oral streptococci and their adhesion to solids. FEMS Microbiol Lett 30:103–106. https://doi.org/10.1111/j.1574-6968.1985.tb00993.x CrossRef

48.

Weerkamp AH, Quirynen M, Marechal M, Van Der Mei HC, Steenberghe DV, Busscher HJ (2009) The role of surface free energy in the early in vivo formation of dental plaque on human enamel and polymeric substrata. Microb Ecol Health Dis 2:11–18. https://doi.org/10.3109/08910608909140196 CrossRef

49.

Rochford ETJ, Subbiahdoss G, Moriarty TF, Poulsson AHC, van der Mei HC, Busscher HJ, Richards RG (2014) An in vitro investigation of bacteria-osteoblast competition on oxygen plasma-modified PEEK. J Biomed Mater Res A 102:4427–4434. https://doi.org/10.1002/jbm.a.35130 CrossRefPubMed

50.

Mai-Prochnow A, Murphy AB, McLean KM, Kong MG, Ostrikov K (2014) Atmospheric pressure plasmas: infection control and bacterial responses. Int J Antimicrob Agents 43:508–517. https://doi.org/10.1016/j.ijantimicag.2014.01.025 CrossRefPubMed

51.

Costerton J (1999) Introduction to biofilm. Int J Antimicrob Agents 11:217–221. https://doi.org/10.1016/s0924-8579(99)00018-7 CrossRefPubMed

52.

Marsh PD, Bradshaw DJ (1995) Dental plaque as a biofilm. J Ind Microbiol 15:169–175. https://doi.org/10.1007/BF01569822 CrossRefPubMed

53.

Jordan RP, Marsh L, Ayre WN, Jones Q, Parkes M, Austin B, Sloan AJ, Waddington RJ (2016) An assessment of early colonisation of implant-abutment metal surfaces by single species and co-cultured bacterial periodontal pathogens. J Dent 53:64–72. https://doi.org/10.1016/j.jdent.2016.07.013 CrossRefPubMed

54.

Tu Y, Ling X, Chen Y, Wang Y, Zhou N, Chen H (2017) Effect of S. mutans and S. sanguinis on growth and adhesion of P. gingivalis and their ability to adhere to different dental materials. Med Sci Monit 23:4539–5445. https://doi.org/10.12659/MSM.904114 CrossRefPubMed

55.

Meza-Siccha AS, Aguilar-Luis MA, Silva-Caso W, Mazulis F, Barragan-Salazar C, Del Valle-Mendoza J (2019) In vitro evaluation of bacterial adhesion and bacterial viability of Streptococcus mutans, Streptococcus sanguinis, and Porphyromonas gingivalis on the abutment surface of titanium and zirconium dental implants. Int J Dent 2019:4292976. https://doi.org/10.1155/2019/4292976 CrossRefPubMedPubMedCentral

56.

Mai-Prochnow A, Clauson M, Hong J, Murphy AB (2016) Gram positive and gram negative bacteria differ in their sensitivity to cold plasma. Sci Rep 6:38610. https://doi.org/10.1038/srep38610 CrossRefPubMedPubMedCentral

Title: Inhibition of bacterial growth on zirconia abutment with a helium cold atmospheric plasma jet treatment
Authors: Yang Yang
Miao Zheng
Yang Yang
Jing Li
Yong-Fei Su
He-Ping Li
Jian-Guo Tan
Publication date: 01-04-2020
Publisher: Springer Berlin Heidelberg
Published in: Clinical Oral Investigations / Issue 4/2020
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-019-03179-2

2024 ASCO Annual Meeting

Springer Medicine

Inhibition of bacterial growth on zirconia abutment with a helium cold atmospheric plasma jet treatment

Abstract

Objectives

Materials and methods

Results

Conclusions

Clinical relevance

2024 ASCO Annual Meeting

Springer Medicine

Abstract

Objectives

Materials and methods

Results

Conclusions

Clinical relevance

Please log in to get access to this content

Other articles of this Issue 4/2020

Comparison of four different suture materials in respect to oral wound healing, microbial colonization, tissue reaction and clinical features—randomized clinical study

Triclosan toothpaste as an adjunct therapy to plaque control in children from periodontitis families: a crossover clinical trial

Relationship between vertical facial pattern and brain structure and shape

Effect of photobiomodulation therapies on the root resorption associated with orthodontic forces: a pilot study using micro computed tomography

Orthodontic cell stress modifies proinflammatory cytokine expression in human PDL cells and induces immunomodulatory effects via TLR-4 signaling in vitro

Effect of non-surgical periodontal therapy on renal function in chronic kidney disease patients with periodontitis: a systematic review and meta-analysis of interventional studies