Korean J Orthod.  2022 Jul;52(4):278-286. 10.4041/kjod21.283.

Variation in adhesion of Streptococcus mutans and Porphyromonas gingivalis in saliva-derived biofilms on raw materials of orthodontic brackets

• Park SH
• Kim K
• Cho S
• Chung DH
• Ahn SJ

• KMID: 2532106
• DOI: http://doi.org/10.4041/kjod21.283

Abstract

Objective
To evaluate differences in the adhesion levels of the most common oral pathogens, Streptococcus mutans and Porphyromonas gingivalis, in human saliva-derived microcosm biofilms with respect to time and raw materials of orthodontic brackets.
Methods
The samples were classified into three groups of bracket materials: 1) monocrystalline alumina ceramic (CR), 2) stainless steel metal (SS), and 3) polycarbonate plastic (PL), and a hydroxyapatite (HA) group was used to mimic the enamel surface. Saliva was collected from a healthy donor, and saliva-derived biofilms were grown on each sample. A realtime polymerase chain reaction was performed to quantitatively evaluate differences in the attachment levels of total bacteria, S. mutans and P. gingivalis at days 1 and 4.
Results
Adhesion of S. mutans and P. gingivalis to CR and HA was higher than the other bracket materials (SS = PL < CR = HA). Total bacteria demonstrated higher adhesion to HA than to bracket materials, but no significant differences in adhesion were observed among the bracket materials (CR = SS = PL < HA). From days 1 to 4, the adhesion of P. gingivalis decreased, while that of S. mutans and total bacteria increased, regardless of material type. onclusions: The higher adhesion of oral pathogens, such as S. mutans and P. gingivalis to CR suggests that the use of CR brackets possibly facilitates gingival inflammation and enamel decalcification during orthodontic treatment.

Keyword

Bracket; Microbiology; Multispecies biofilms; Oral pathogen

Figure

• 

  Figure 1 Scanning electron microscope images of materials used in this study. The images were taken at 3,000× magnification. A, Monocrystalline alumina ceramic. B, Stainless steel metal. C, Polycarbonate plastic. D, Hydroxyapatite.

Reference

1. Low B, Lee W, Seneviratne CJ, Samaranayake LP, Hägg U. 2011; Ultrastructure and morphology of biofilms on thermoplastic orthodontic appliances in 'fast' and 'slow' plaque formers. Eur J Orthod. 33:577–83. DOI: 10.1093/ejo/cjq126. PMID: 21187528. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=80053464335&origin=inward.

2. Naranjo AA, Triviño ML, Jaramillo A, Betancourth M, Botero JE. 2006; Changes in the subgingival microbiota and periodontal parameters before and 3 months after bracket placement. Am J Orthod Dentofacial Orthop. 130:275.e17–22. DOI: 10.1016/j.ajodo.2005.10.022. PMID: 16979483. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=33748440367&origin=inward.

3. Lucchese A, Gherlone E. 2013; Prevalence of white-spot lesions before and during orthodontic treatment with fixed appliances. Eur J Orthod. 35:664–8. DOI: 10.1093/ejo/cjs070. PMID: 23045306. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=84885082210&origin=inward.

4. Eliades T, Eliades G, Brantley WA. 1995; Microbial attachment on orthodontic appliances: I. Wettability and early pellicle formation on bracket materials. Am J Orthod Dentofacial Orthop. 108:351–60. DOI: 10.1016/S0889-5406(95)70032-3. PMID: 7572846. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0029393618&origin=inward.

5. Lim BS, Lee SJ, Lee JW, Ahn SJ. 2008; Quantitative analysis of adhesion of cariogenic streptococci to orthodontic raw materials. Am J Orthod Dentofacial Orthop. 133:882–8. DOI: 10.1016/j.ajodo.2006.07.027. PMID: 18538253. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=44449096172&origin=inward.

6. Komori R, Sato T, Takano-Yamamoto T, Takahashi N. 2012; Microbial composition of dental plaque microflora on first molars with orthodontic bands and brackets, and the acidogenic potential of these bacteria. J Oral Biosci. 54:107–12. DOI: 10.1016/j.job.2012.01.009. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=84867575089&origin=inward.

7. Kolenbrander PE, Palmer RJ Jr, Periasamy S, Jakubovics NS. 2010; Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol. 8:471–80. DOI: 10.1038/nrmicro2381. PMID: 20514044. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=77953620116&origin=inward.

8. Haririan H, Andrukhov O, Bertl K, Lettner S, Kierstein S, Moritz A, et al. 2014; Microbial analysis of subgingival plaque samples compared to that of whole saliva in patients with periodontitis. J Periodontol. 85:819–28. DOI: 10.1902/jop.2013.130306. PMID: 24144271. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=84903436418&origin=inward.

9. Williams DL, Bloebaum RD. 2010; Observing the biofilm matrix of Staphylococcus epidermidis ATCC 35984 grown using the CDC biofilm reactor. Microsc Microanal. 16:143–52. DOI: 10.1017/S143192760999136X. PMID: 20205969. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=77952542903&origin=inward.

10. Good RJ. 1992; Contact angle, wetting, and adhesion: a critical review. J Adhes Sci Technol. 6:1269–302. DOI: 10.1163/156856192X00629. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=84953125819&origin=inward.

11. McBain AJ, Sissons C, Ledder RG, Sreenivasan PK, De Vizio W, Gilbert P. 2005; Development and characterization of a simple perfused oral microcosm. J Appl Microbiol. 98:624–34. DOI: 10.1111/j.1365-2672.2004.02483.x. PMID: 15715865. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=14844303548&origin=inward.

12. Viana CS, Maske TT, Signori C, VAN DE Sande FH, Oliveira EF, Cenci MS. 2021; Influence of caries activity and number of saliva donors: mineral and microbiological responses in a microcosm biofilm model. J Appl Oral Sci. 29:e20200778. DOI: 10.1590/1678-7757-2020-0778. PMID: 34495103. PMCID: PMC8425900. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=85114852064&origin=inward.

13. Shu M, Browngardt CM, Chen YY, Burne RA. 2003; Role of urease enzymes in stability of a 10-species oral biofilm consortium cultivated in a constant-depth film fermenter. Infect Immun. 71:7188–92. DOI: 10.1128/IAI.71.12.7188-7192.2003. PMID: 14638814. PMCID: PMC308945. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0345283039&origin=inward.

14. Donlan RM, Piede JA, Heyes CD, Sanii L, Murga R, Edmonds P, et al. 2004; Model system for growing and quantifying Streptococcus pneumoniae biofilms in situ and in real time. Appl Environ Microbiol. 70:4980–8. DOI: 10.1128/AEM.70.8.4980-4988.2004. PMID: 15294838. PMCID: PMC492445. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=4143132359&origin=inward.

15. An JS, Kim K, Cho S, Lim BS, Ahn SJ. 2017; Compositional differences in multi-species biofilms formed on various orthodontic adhesives. Eur J Orthod. 39:528–33. DOI: 10.1093/ejo/cjw089. PMID: 28339597. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=85028725118&origin=inward.

16. Rudney JD, Chen R, Lenton P, Li J, Li Y, Jones RS, et al. 2012; A reproducible oral microcosm biofilm model for testing dental materials. J Appl Microbiol. 113:1540–53. DOI: 10.1111/j.1365-2672.2012.05439.x. PMID: 22925110. PMCID: PMC3501590. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=84869872306&origin=inward.

17. Park JW, An JS, Lim WH, Lim BS, Ahn SJ. 2019; Microbial changes in biofilms on composite resins with different surface roughness: an in vitro study with a multispecies biofilm model. J Prosthet Dent. 122:493.e1–493.e8. DOI: 10.1016/j.prosdent.2019.08.009. PMID: 31648793. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=85073918757&origin=inward.

18. Yin JL, Shackel NA, Zekry A, McGuinness PH, Richards C, Putten KV, et al. 2001; Real-time reverse transcriptase-polymerase chain reaction (RT-PCR) for measurement of cytokine and growth factor mRNA expression with fluorogenic probes or SYBR Green I. Immunol Cell Biol. 79:213–21. DOI: 10.1046/j.1440-1711.2001.01002.x. PMID: 11380673. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0034993341&origin=inward.

19. Fournier A, Payant L, Bouclin R. 1998; Adherence of Streptococcus mutans to orthodontic brackets. Am J Orthod Dentofacial Orthop. 114:414–7. DOI: 10.1016/S0889-5406(98)70186-6. PMID: 9790325. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0032184822&origin=inward.

20. Ahn SJ, Kho HS, Lee SW, Nahm DS. 2002; Roles of salivary proteins in the adherence of oral streptococci to various orthodontic brackets. J Dent Res. 81:411–5. DOI: 10.1177/154405910208100611. PMID: 12097434. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0035983426&origin=inward.

21. Lindel ID, Elter C, Heuer W, Heidenblut T, Stiesch M, Schwestka-Polly R, et al. 2011; Comparative analysis of long-term biofilm formation on metal and ceramic brackets. Angle Orthod. 81:907–14. DOI: 10.2319/102210-616.1. PMID: 21542722. PMCID: PMC8916195. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=80052482361&origin=inward.

22. Watanabe I, Watanabe E. 2003; Surface changes induced by fluoride prophylactic agents on titanium-based orthodontic wires. Am J Orthod Dentofacial Orthop. 123:653–6. DOI: 10.1016/S0889-5406(03)00197-5. PMID: 12806345. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0038507442&origin=inward.

23. McBain AJ. 2009; In vitro biofilm models: an overview. Adv Appl Microbiol. 69:99–132. DOI: 10.1016/S0065-2164(09)69004-3. PMID: 19729092. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=69249171333&origin=inward.

24. Nyvad B, Fejerskov O. 1987; Scanning electron microscopy of early microbial colonization of human enamel and root surfaces in vivo. Scand J Dent Res. 95:287–96. DOI: 10.1111/j.1600-0722.1987.tb01844.x. PMID: 3476984. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=84989593861&origin=inward.

25. Quirynen M, Marechal M, Busscher HJ, Weerkamp AH, Darius PL, van Steenberghe D. 1990; The influence of surface free energy and surface roughness on early plaque formation. An in vivo study in man. J Clin Periodontol. 17:138–44. DOI: 10.1111/j.1600-051X.1990.tb01077.x. PMID: 2319000. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0025054981&origin=inward.

26. Busscher HJ, van Pelt AWJ, de Boer P, de Jong HP, Arends J. 1984; The effect of surface roughening of polymers on measured contact angles of liquids. Colloids Surf. 9:319–31. DOI: 10.1016/0166-6622(84)80175-4. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0021423982&origin=inward.

27. An YH, Friedman RJ. 1998; Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. J Biomed Mater Res. 43:338–48. DOI: 10.1002/(SICI)1097-4636(199823)43:3<338::AID-JBM16>3.0.CO;2-B. PMID: 9730073.

28. ten Cate JM. 2006; Biofilms, a new approach to the microbiology of dental plaque. Odontology. 94:1–9. DOI: 10.1007/s10266-006-0063-3. PMID: 16998612. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=33749059765&origin=inward.

29. Bollen CM, Lambrechts P, Quirynen M. 1997; Comparison of surface roughness of oral hard materials to the threshold surface roughness for bacterial plaque retention: a review of the literature. Dent Mater. 13:258–69. DOI: 10.1016/S0109-5641(97)80038-3. PMID: 11696906. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0031173323&origin=inward.

30. Simonson LG, Reiher DA. 1981; Effect of human saliva and various compounds on the adsorption of the bacterium Streptococcus mutans to hydroxyapatite. Arch Oral Biol. 26:143–6. DOI: 10.1016/0003-9969(81)90085-6. PMID: 6944026. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=0019419122&origin=inward.

31. Suzuki N, Yoshida A, Nakano Y. 2005; Quantitative analysis of multi-species oral biofilms by TaqMan Real-Time PCR. Clin Med Res. 3:176–85. DOI: 10.3121/cmr.3.3.176. PMID: 16160072. PMCID: PMC1237159. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=27744600265&origin=inward.

32. Ahn SJ, Burne RA. 2007; Effects of oxygen on biofilm formation and the AtlA autolysin of Streptococcus mutans. J Bacteriol. 189:6293–302. DOI: 10.1128/JB.00546-07. PMID: 17616606. PMCID: PMC1951938. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=34548480696&origin=inward.

33. Kirthiga M, Murugan M, Saikia A, Kirubakaran R. 2019; Risk factors for early childhood caries: a systematic review and meta-analysis of case control and cohort studies. Pediatr Dent. 41:95–112. PMID: 30992106. PMCID: PMC7100045. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=85064973342&origin=inward.

34. Wang BY, Lu T, Cai Q, Ho MH, Sheng S, Meng HW, et al. 2021; Potential microbiological risk factors associated with periodontitis and periodontal health disparities. Front Cell Infect Microbiol. 11:789919. DOI: 10.3389/fcimb.2021.789919. PMID: 34869082. PMCID: PMC8637773. PMID: 940959c0bbb24e50acad281cfc84c307. PMID: https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=85120677662&origin=inward.