Abstract
We investigated whether irradiation with 405-nm blue LED light could inhibit the growth of not only single- but dual-species biofilms formed by Candida albicans and Streptococcus mutans on denture base resin and cause the alteration in gene expression related to adhesion and biofilm formation. C. albicans and S. mutans single-/dual-species biofilms were formed on the denture base specimens. The biofilms were irradiated with 405-nm blue LED light (power density output: 280 mW/cm2) for 0 (control) and 40 min. Dual-species biofilms were analyzed using CFU assay and fluorescence microscopy, and single-/dual-species biofilms were analyzed using alamarBlue assays and gene expression analysis. To assess the inhibitory effect of irradiation on dual-species biofilms, specimens after irradiation were aerobically incubated for 12 h. After incubation, the inhibition of growth was assessed using CFU assays and fluorescence microscopy. Data were analyzed using the Mann–Whitney U or Student’s t test (p < 0.05). Irradiation produced a significant inhibitory effect on biofilms. Fluorescence microscopy revealed that almost all C. albicans and S. mutans cells were killed by irradiation, and there was no notable difference in biofilm thickness immediately after irradiation and after irradiation and incubation for 12 h. alamarBlue assays indicated the growth of the biofilms was inhibited for 12–13 h. The expression of genes associated with adhesion and biofilm formation—als1 in C. albicans and ftf, gtfC, and gtfB in S. mutans—significantly reduced by irradiation. Irradiation with 405-nm blue LED light effectively inhibited the growth of C. albicans and S. mutans dual-species biofilms for 12 h.
Similar content being viewed by others
References
Gendreau L, Loewy ZG (2011) Epidemiology and etiology of denture stomatitis. J Prosthodont 20(4):251–260. https://doi.org/10.1111/j.1532-849X.2011.00698.x
Nikawa H, Hamada T, Yamamoto T (1998) Denture plaque–past and recent concerns. J Dent 26(4):299–304. https://doi.org/10.1016/s0300-5712(97)00026-2
Salerno C, Pascale M, Contaldo M, Esposito V, Busciolano M, Milillo L et al (2011) Candida-associated denture stomatitis. Med Oral Patol Oral Cir Bucal 16(2):e139–e143. https://doi.org/10.4317/medoral.16.e139
Mantzourani M, Gilbert SC, Fenlon M, Beighton D (2010) Non-oral bifidobacteria and the aciduric microbiota of the denture plaque biofilm. Mol Oral Microbiol 25(3):190–199. https://doi.org/10.1111/j.2041-1014.2009.00565.x
Yassin SA, German MJ, Rolland SL, Rickard AH, Jakubovics NS (2016) Inhibition of multispecies biofilms by a fluoride-releasing dental prosthesis copolymer. J Dent 48:62–70. https://doi.org/10.1016/j.jdent.2016.03.001
Sudbery PE (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9(10):737–748. https://doi.org/10.1038/nrmicro2636
Sánchez-Vargas LO, Estrada-Barraza D, Pozos-Guillen AJ, Rivas-Caceres R (2013) Biofilm formation by oral clinical isolates of Candida species. Arch Oral Biol 58(10):1318–1326. https://doi.org/10.1016/j.archoralbio.2013.06.006
Abrantes P, Africa CWJ (2020) Measuring Streptococcus mutans, Streptococcus sanguinis and Candida albicans biofilm formation using a real-time impedance-based system. J Microbiol Methods 169:105815. https://doi.org/10.1016/j.mimet.2019.105815
Falsetta ML, Klein MI, Colonne PM, Scott-Anne K, Gregoire S, Pai CH et al (2014) Symbiotic relationship between Streptococcus mutans and Candida albicans synergizes virulence of plaque biofilms in vivo. Infect Immun 82(5):1968–1981. https://doi.org/10.1128/iai.00087-14
Nikawa H, Egusa H, Makihira S, Yamashiro H, Fukushima H, Jin C et al (2001) Alteration of the coadherence of Candida albicans with oral bacteria by dietary sugars. Oral Microbiol Immunol 16(5):279–283. https://doi.org/10.1034/j.1399-302x.2001.016005279.x
Rocha EP, Francisco SB, Del Bel Cury AA, Cury JA (2003) Longitudinal study of the influence of removable partial denture and chemical control on the levels of Streptococcus mutans in saliva. J Oral Rehabil 30(2):131–138. https://doi.org/10.1046/j.1365-2842.2003.01015.x
Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2(2):114–122. https://doi.org/10.1038/nrd1008
Jagger DC, Harrison A (1995) Denture cleansing–the best approach. Br Dent J 178(11):413–417. https://doi.org/10.1038/sj.bdj.4808788
Moussa AR, Dehis WM, Elboraey AN, ElGabry HS (2016) A comparative clinical study of the effect of denture cleansing on the surface roughness and hardness of two denture base materials. Open Access Maced J Med Sci 4(3):476–481. https://doi.org/10.3889/oamjms.2016.089
Freitas-Fernandes FS, Cavalcanti YW, Ricomini Filho AP, Silva WJ, Del Bel Cury AA, Bertolini MM (2014) Effect of daily use of an enzymatic denture cleanser on Candida albicans biofilms formed on polyamide and poly(methyl methacrylate) resins: an in vitro study. J Prosthet Dent 112(6):1349–1355. https://doi.org/10.1016/j.prosdent.2014.07.004
Tsutsumi-Arai C, Arai Y, Terada-Ito C, Imamura T, Tatehara S, Ide S, et al. (2021) Microbicidal effect of 405-nm blue LED light on Candida albicans and Streptococcus mutans dual-species biofilms on denture base resin. Lasers Med Sci. doi: https://doi.org/10.1007/s10103-021-03323-z
Tsutsumi-Arai C, Arai Y, Terada-Ito C, Takebe Y, Ide S, Umeki H et al (2019) Effectiveness of 405-nm blue LED light for degradation of Candida biofilms formed on PMMA denture base resin. Lasers Med Sci 34(7):1457–1464. https://doi.org/10.1007/s10103-019-02751-2
Carrera ET, Dias HB, Corbi SCT, Marcantonio RAC, Bernardi ACA, Bagnato VS et al (2016) The application of antimicrobial photodynamic therapy (aPDT) in dentistry: a critical review. Laser Phys 26(12):123001. https://doi.org/10.1088/1054-660x/26/12/123001
Abegg MA, Alabarse PV, Casanova A, Hoscheid J, Salomon TB, Hackenhaar FS et al (2010) Response to oxidative stress in eight pathogenic yeast species of the genus Candida. Mycopathologia 170(1):11–20. https://doi.org/10.1007/s11046-010-9294-5
Nikinmaa S, Alapulli H, Auvinen P, Vaara M, Rantala J, Kankuri E et al (2020) Dual-light photodynamic therapy administered daily provides a sustained antibacterial effect on biofilm and prevents Streptococcus mutans adaptation. PLoS ONE 15(5):e0232775. https://doi.org/10.1371/journal.pone.0232775
Fukui M, Yoshioka M, Satomura K, Nakanishi H, Nagayama M (2008) Specific-wavelength visible light irradiation inhibits bacterial growth of Porphyromonas gingivalis. J Periodontal Res 43(2):174–178. https://doi.org/10.1111/j.1600-0765.2007.01009.x
Tsutsumi C, Takakuda K, Wakabayashi N (2016) Reduction of Candida biofilm adhesion by incorporation of prereacted glass ionomer filler in denture base resin. J Dent 44:37–43. https://doi.org/10.1016/j.jdent.2015.11.010
Tsutsumi-Arai C, Takakusaki K, Arai Y, Terada-Ito C, Takebe Y, Imamura T et al (2019) Grapefruit seed extract effectively inhibits the Candida albicans biofilms development on polymethyl methacrylate denture-base resin. PLoS ONE 14(5):e0217496. https://doi.org/10.1371/journal.pone.0217496
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Ellepola K, Liu Y, Cao T, Koo H, Seneviratne CJ (2017) Bacterial GtfB augments Candida albicans accumulation in cross-kingdom biofilms. J Dent Res 96(10):1129–1135. https://doi.org/10.1177/0022034517714414
Septiana S, Bachtiar BM, Yuliana ND, Wijaya CH (2019) Cajuputs candy impairs Candida albicans and Streptococcus mutans mixed biofilm formation in vitro. F1000Res 8:1923. doi: https://doi.org/10.12688/f1000research.20700.2
Shemesh M, Tam A, Steinberg D (2007) Expression of biofilm-associated genes of Streptococcus mutans in response to glucose and sucrose. J Med Microbiol 56(Pt 11):1528–1535. https://doi.org/10.1099/jmm.0.47146-0
Abastabar M, Hosseinpoor S, Hedayati MT, Shokohi T, Valadan R, Mirhendi H et al (2016) Hyphal wall protein 1 gene: a potential marker for the identification of different Candida species and phylogenetic analysis. Curr Med Mycol 2(4):1–8. https://doi.org/10.18869/acadpub.cmm.2.4.1
García-Sánchez S, Aubert S, Iraqui I, Janbon G, Ghigo JM, d’Enfert C (2004) Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot Cell 3(2):536–545. https://doi.org/10.1128/ec.3.2.536-545.2004
Nobile CJ, Mitchell AP (2006) Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol 8(9):1382–1391. https://doi.org/10.1111/j.1462-5822.2006.00761.x
Berman J, Sudbery PE (2002) Candida Albicans: a molecular revolution built on lessons from budding yeast. Nat Rev Genet 3(12):918–930. https://doi.org/10.1038/nrg948
Furuya K, Niki H (2010) The DNA damage checkpoint regulates a transition between yeast and hyphal growth in Schizosaccharomyces japonicus. Mol Cell Biol 30(12):2909–2917. https://doi.org/10.1128/mcb.00049-10
McCall AD, Pathirana RU, Prabhakar A, Cullen PJ, Edgerton M (2019) Candida albicans biofilm development is governed by cooperative attachment and adhesion maintenance proteins. NPJ Biofilms Microbiomes 5(1):21. https://doi.org/10.1038/s41522-019-0094-5
Nobile CJ, Schneider HA, Nett JE, Sheppard DC, Filler SG, Andes DR et al (2008) Complementary adhesin function in C. albicans biofilm formation. Curr Biol 18(14):1017–24. https://doi.org/10.1016/j.cub.2008.06.034
O’Connor L, Lahiff S, Casey F, Glennon M, Cormican M, Maher M (2005) Quantification of ALS1 gene expression in Candida albicans biofilms by RT-PCR using hybridisation probes on the LightCycler. Mol Cell Probes 19(3):153–162. https://doi.org/10.1016/j.mcp.2004.10.007
Roudbarmohammadi S, Roudbary M, Bakhshi B, Katiraee F, Mohammadi R, Falahati M (2016) ALS1 and ALS3 gene expression and biofilm formation in Candida albicans isolated from vulvovaginal candidiasis. Adv Biomed Res 5:105. https://doi.org/10.4103/2277-9175.183666
Nam YJ, Hwang YS (2021) Antibacterial and antioxidant effect of ethanol extracts of Terminalia chebula on Streptococcus mutans. Clin Exp Dent Res. https://doi.org/10.1002/cre2.467
Wexler DL, Hudson MC, Burne RA (1993) Streptococcus mutans fructosyltransferase (ftf) and glucosyltransferase (gtfBC) operon fusion strains in continuous culture. Infect Immun 61(4):1259–1267. https://doi.org/10.1128/iai.61.4.1259-1267.1993
Huffines JT, Scoffield JA (2020) Disruption of Streptococcus mutans and Candida albicans synergy by a commensal streptococcus. Sci Rep 10(1):19661. https://doi.org/10.1038/s41598-020-76744-5
Srivastava N, Ellepola K, Venkiteswaran N, Chai LYA, Ohshima T, Seneviratne CJ (2020) Lactobacillus plantarum 108 inhibits Streptococcus mutans and Candida albicans mixed-species biofilm formation. Antibiotics (Basel) 9(8):478. https://doi.org/10.3390/antibiotics9080478
Acknowledgements
We thank Osada Electric Co. Ltd. for technical support concerning an irradiation device.
Funding
This work was supported by JSPS KAKENHI (Grant Number 20K18649). The funder was not involved in the study design, collection, analysis, interpretation of data, the writing of this report, or the decision to submit the paper for publication.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
None.
Conflict of interest
The authors declare no competing interests.
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
Tsutsumi-Arai, C., Arai, Y., Terada-Ito, C. et al. Inhibitory effect of 405-nm blue LED light on the growth of Candida albicans and Streptococcus mutans dual-species biofilms on denture base resin. Lasers Med Sci 37, 2311–2319 (2022). https://doi.org/10.1007/s10103-022-03507-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10103-022-03507-1