Abstract
The potential anti-cariogenic effect of blue light was evaluated using an oral biofilm model. Two species, Streptococcus mutans and Streptococcus sanguinis, were cultivated ex vivo on bovine enamel blocks for 24 h, either separately or mixed together, then exposed to blue light (wavelengths 400–500 nm) using 112 J/cm2. Twenty four or 48 h after exposure to light the biofilm structure and biomass were characterized and quantified using SEM and qPCR, respectively. Bacterial viability was analyzed by CLSM using live/dead bacterial staining. Gene expression was examined by RT-qPCR. After exposure to light, S. mutans biomass in mono-species biofilm was increased mainly by dead bacteria, relative to control. However, the bacterial biomass of S. mutans when grown in mixed biofilm and of S. sanguinis in mono-species biofilm was reduced after light exposure, with no significant change in viability when compared to control. Furthermore, when grown separately, an upregulation of gene expression related to biofilm formation of S. mutans, and downregulation of similar genes of S. sanguinis, were measured 24 h after exposure to blue light. However, in mixed biofilm, a downregulation of those genes in both species was observed, although not significant in S. mutans. In conclusion, blue light seems to effectively alter the bacterial biomass by reducing the viability and virulence characteristics in both bacterial species and may promote the anti-cariogenic balance between them, when grown in a mixed biofilm. Therefore, exposure of oral biofilm to blue light has the potential to serve as a complementary approach in preventive dentistry.
Similar content being viewed by others
References
Pitts NB, Zero DT, Marsh PD, Ekstrand K, Weintraub JA, Ramos-Gomez F, Tagami J, Twetman S, Tsakos G, Ismail A (2017) Dental caries. Nat Rev Dis Primers 3:17030
Marsh PD (2005) Dental plaque: biological significance of a biofilm and community life-style. J Clin Periodontol 32(Suppl 6):7–15
Steinberg D, Moreinos D, Featherstone J, Shemesh M, Feuerstein O (2008) Genetic and physiological effects of noncoherent visible light combined with hydrogen peroxide on Streptococcus mutans in biofilm. Antimicrob Agents Chemother 52(7):2626–2631
Larsen T, Fiehn NE (2017) Dental biofilm infections – an update. APMIS 125(4):376–384
Niven CF Jr, White JC (1946) A study of streptococci associated with subacute bacterial endocarditis. J Bacteriol 51(6):790
Ge Y, Caufield PW, Fisch GS, Li Y (2008) Streptococcus mutans and Streptococcus sanguinis colonization correlated with caries experience in children. Caries Res 42(6):444–448
Valdebenito B, Tullume-Vergara PO, González W, Kreth J, Giacaman RA (2017) In silico analysis of the competition between Streptococcus sanguinis and Streptococcus mutans in the dental biofilm. Mol Oral Microbiol 33(2):168–180
Kreth J, Merritt J, Qi F (2009) Bacterial and host interactions of oral streptococci. DNA Cell Biol 28(8):397–403
Feuerstein O, Persman N, Weiss EI (2004) Phototoxic effect of visible light on Porphyromonas gingivalis and Fusobacterium nucleatum: An in Vitro Study. Photochem Photobiol 80(3):412–415
Chebath-Taub D, Steinberg D, Featherstone JD, Feuerstein O (2012) Influence of blue light on Streptococcus mutans re-organization in biofilm. J Photochem Photobiol B 116:75–78
Sol A, Feuerstein O, Featherstone JD, Steinberg D (2011) Effect of sublethal CO2 laser irradiation on gene expression of Streptococcus mutans immobilized in a biofilm. Caries Res 45(4):361–369
Cohen-Berneron J, Steinberg D, Featherstone JD, Feuerstein O (2016) Sustained effects of blue light on Streptococcus mutans in regrown biofilm. Lasers Med Sci 31(3):445–452
Feuerstein O, Assad R, Koren E, Ginsburg I, Weiss EI, Houri-Haddad Y (2011) Visible light promotes interleukin-10 secretion by sublethal fluences. Photomed Laser Surg. 29(9):627–633
McCormack SM, Fried D, Featherstone JD, Glena RE, Seka W (1995) Scanning electron microscope observations of CO2 laser effects on dental enamel. J Dent Res 74(10):1702–1708
Periasamy S, Kolenbrander PE (2009) Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J Bacteriol 191(22):6804–6811
Assaf D, Steinberg D, Shemesh M (2015) Lactose triggers biofilm formation by Streptococcus mutans. Int Dairy J 42:51–57
Shemesh M, Tam A, Aharoni R, Steinberg D (2010) Genetic adaptation of Streptococcus mutans during biofilm formation on different types of surfaces. BMC Microbiol 10:51
Feldman M, Al-Quntar A, Polacheck I, Friedman M, Steinberg D (2014) Therapeutic potential of thiazolidinedione-8 as an antibiofilm agent against Candida albicans. PLoS One 9(5):e93225
Ramage G, Saville SP, Wickes BL, López-Ribot JL (2002) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68(11):5459–5463
Shemesh M, Tam A, Steinberg D (2007) Differential gene expression profiling of Streptococcus mutans cultured under biofilm and planktonic conditions. Microbiology 153(Pt 5):1307–1317
Shemesh M, Tam A, Feldman M, Steinberg D (2006) Differential expression profiles of Streptococcus mutans ftf, gtf and vicR genes in the presence of dietary carbohydrates at early and late exponential growth phases. Carbohydr Res 341(12):2090–2097
Kreth J, Giacaman RA, Raghavan R, Merritt J (2017) The road less traveled – defining molecular commensalism with Streptococcus sanguinis. Mol Oral Microbiol 32(3):181–196
Cieplik F, Kara E, Muehler D, Enax J, Hiller KA, Maisch T, Buchalla W (2018) Antimicrobial efficacy of alternative compounds for use in oral care toward biofilms from caries-associated bacteria in vitro. Microbiologyopen e00695
Krzyściak W, Jurczak A, Kościelniak D, Bystrowska B, Skalniak A (2014) The virulence of Streptococcus mutans and the ability to form biofilms. Eur J Clin Microbiol Infect Dis 33(4):499–515
Rossoni RD, Velloso MDS, de Barros PP, de Alvarenga JA, Santos JDD, Santos Prado ACCD, Ribeiro FC, Anbinder AL, Junqueira JC (2018) Inhibitory effect of probiotic Lactobacillus supernatants from the oral cavity on Streptococcus mutans biofilms. Microb Pathog 123:361–367
Souza JGS, Cury JA, Ricomini Filho AP, Feres M, Faveri M, Barão VAR (2018) Effect of sucrose on biofilm formed in situ on titanium material. J Periodontol
Feuerstein O (2012) Light therapy: complementary antibacterial treatment of oral biofilm. Adv Dent Res 24(2):103–107
Palma ALDR, Ramos LP, Domingues N, Back-Brito GN, de Oliveira LD, Pereira CA, Jorge AOC (2018) Biofilms of Candida albicans and Streptococcus sanguinis and their susceptibility to antimicrobial effects of photodynamic inactivation. Photodiagnosis Photodyn Ther pii S1572-1000(17):30455–30456
Hauser-Gerspach I, Stübinger S, Meyer J (2010) Bactericidal effects of different laser systems on bacteria adhered to dental implant surfaces: an in vitro study comparing zirconia with titanium. Clin Oral Implants Res 21(3):277–283
Uchinuma S, Shimada Y, Matin K, Hosaka K, Yoshiyama M, Sumi Y, Tagami J (2018) Effects of UVB and UVC irradiation on cariogenic bacteria in vitro. Lasers Med Sci. https://doi.org/10.1007/s10103-018-2685-4
Giusti JS, Santos-Pinto L, Pizzolito AC, Helmerson K, Carvalho-Filho E, Kurachi C, Bagnato VS (2008) Antimicrobial photodynamic action on dentin using a light-emitting diode light source. Photomed Laser Surg 26(4):281–287
Hakimiha N, Khoei F, Bahador A, Fekrazad R (2014) The susceptibility of Streptococcus mutans to antibacterial photodynamic therapy: a comparison of two different photosensitizers and light sources. J Appl Oral Sci 22(2):80–84
Pereira CA, Costa AC, Carreira CM, Junqueira JC, Jorge AO (2013) Photodynamic inactivation of Streptococcus mutans and Streptococcus sanguinis biofilms in vitro. Lasers Med Sci 28(3):859–864
Soria-Lozano P, Gilaberte Y, Paz-Cristobal MP, Pérez-Artiaga L, Lampaya-Pérez V, Aporta J, Pérez-Laguna V, García-Luque I, Revillo MJ, Rezusta A (2015) In vitro effect photodynamic therapy with differents photosensitizers on cariogenic microorganisms. BMC Microbiol 15:187
Pérez-Laguna V, Pérez-Artiaga L, Lampaya-Pérez V, López SC, García-Luque I, Revillo MJ, Nonell S, Gilaberte Y, Rezusta A (2017) Comparative effect of photodynamic therapy on separated or mixed cultures of Streptococcus mutans and Streptococcus sanguinis. Photodiagnosis Photodyn Ther 19:98–102
Ichinose-Tsuno A, Aoki A, Takeuchi Y, Kirikae T, Shimbo T, Lee MC, Yoshino F, Maruoka Y, Itoh T, Ishikawa I, Izumi Y (2014) Antimicrobial photodynamic therapy suppresses dental plaque formation in healthy adults: a randomized controlled clinical trial. BMC Oral Health 14:152
Feuerstein O, Ginsburg I, Dayan E, Veler D, Weiss EI (2005) Mechanism of visible light phototoxicity on Porphyromonas gingivalis and Fusobacterium nucleatum. Photochem Photobiol 81(5):1186–1189
Sterer N, Feuerstein O (2005) Effect of visible light on malodour production by mixed oral microflora. J Med Microbiol 54(Pt 12):1225–1229
Khaengraeng R, Reed RH (2005) Oxygen and photoinactivation of Escherichia coli in UVA and sunlight. J Appl Microbiol 99(1):39–50
Lubart R, Lipovski A, Nitzan Y, Friedmann H (2011) A possible mechanism for the bactericidal effect of visible light. Laser Ther 20(1):17–22
Storz G, Imlay JA (1999) Oxidative stress. Curr Opin Microbiol 2(2):188–194
Tardu M, Bulut S, Kavakli IH (2017) MerR and ChrR mediate blue light induced photo-oxidative stress response at the transcriptional level in Vibrio cholerae. Sci Rep 18(7):40817
Chui C, Hiratsuka K, Aoki A, Takeuchi Y, Abiko Y, Izumi Y (2012) Blue LED inhibits the growth of Porphyromonas gingivalis by suppressing the expression of genes associated with DNA replication and cell division. Lasers Surg Med. 44(10):856–864
Kreth J, Merritt J, Shi W, Qi F (2005) Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J Bacteriol 187(21):7193–7203
Kuramitsu HK, He X, Lux R, Anderson MH, Shi W (2007) Interspecies interactions within oral microbial communities. Microbiol Mol Biol Rev 71(4):653–670
Funding
This work was partially supported by the United States-Israel Binational Science Foundation (BSF) grant (#2013445).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed consent
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Vaknin, M., Steinberg, D., Featherstone, J.D. et al. Exposure of Streptococcus mutans and Streptococcus sanguinis to blue light in an oral biofilm model. Lasers Med Sci 35, 709–718 (2020). https://doi.org/10.1007/s10103-019-02903-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10103-019-02903-4