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01-03-2022 | Candida Balanitis | Original Article

Microbicidal effect of 405-nm blue LED light on Candida albicans and Streptococcus mutans dual-species biofilms on denture base resin

Authors: Chiaki Tsutsumi-Arai, Yuki Arai, Chika Terada-Ito, Takahiro Imamura, Seiko Tatehara, Shinji Ide, Noriyuki Wakabayashi, Kazuhito Satomura

Published in: Lasers in Medical Science | Issue 2/2022

Abstract

This study investigated: (1) the microbicidal effect of 405-nm blue LED light irradiation on biofilm formed by Candida albicans hyphae and Streptococcus mutans under dual-species condition on denture base resin, (2) the generation of intracellular reactive oxygen species (ROS) induced by irradiation, and (3) the existence of intracellular porphyrins, which act as a photosensitizer. Denture base resin specimens were prepared and C. albicans and S. mutans dual-species biofilms were allowed to form on the specimens. The biofilms were irradiated with 405-nm blue LED light and analyzed using the colony-forming unit assay, fluorescence microscopy, and scanning electron microscopy (SEM). Single-species biofilms of C. albicans and S. mutans formed on the specimens were irradiated with 405-nm blue LED light. After the irradiation, the intracellular ROS levels in C. albicans and S. mutans cells were measured. In addition, the level of intracellular porphyrins in C. albicans and S. mutans were measured. Irradiation for more than 30 min significantly inhibited the colony formation ability of C. albicans and S. mutans. Fluorescence microscopy revealed that almost all C. albicans and S. mutans cells were killed by irradiation. SEM images showed various cell damage patterns. Irradiation led to the generation of intracellular ROS and porphyrins were present in both C. albicans and S. mutans cells. In conclusion, irradiation with 405-nm blue light-emitting diode light for 40 min effectively disinfect C. albicans hyphae and S. mutans dual-species biofilms and possibly react with intracellular porphyrins resulting in generation of ROS in each microorganism.

Cumming CG, Wight C, Blackwell CL, Wray D (1990) Denture stomatitis in the elderly. Oral Microbiol Immunol 5(2):82–85. https://doi.org/10.1111/j.1399-302X.1990.tb00232.xCrossRefPubMed

Arendorf TM, Walker DM (1987) Denture stomatitis: a review. J Oral Rehabil 14(3):217–227. https://doi.org/10.1111/j.1365-2842.1987.tb00713.xCrossRefPubMed

Budtz-Jörgensen E, Stenderup A, Grabowski M (1975) An epidemiologic study of yeasts in elderly denture wearers. Commun Dent Oral Epidemiol 3(3):115–119. https://doi.org/10.1111/j.1600-0528.1975.tb00291.xCrossRef

Bergendal T, Holmberg K (1982) Studies of Candida serology in denture stomatitis patients. Eur J Oral Sci 90(4):315–322. https://doi.org/10.1111/j.1600-0722.1982.tb00743.xCrossRef

Webb BC, Thomas CJ, Willcox MDP, Harty DWS, Knox KW (1998) Candida-associated denture stomatitis. Aetiology and management: a review: part1. Factors influencing distribution of candida species in the oral cavity. Australian Dental Journal 43(1):45–50. https://doi.org/10.1111/j.1834-7819.1998.tb00152.xCrossRefPubMed

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.2016.03.001CrossRefPubMed

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.xCrossRefPubMed

Sudbery PE (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9(10):737–748. https://doi.org/10.1038/nrmicro2636CrossRefPubMed

Morse DJ, Wilson MJ, Wei X, Bradshaw DJ, Lewis MAO, Williams DW (2019) Modulation of Candida albicans virulence in in vitro biofilms by oral bacteria. Lett Appl Microbiol 68(4):337–343. https://doi.org/10.1111/lam.13145CrossRefPubMedPubMedCentral

10.

Xu H, Sobue T, Bertolini M, Thompson A, Dongari-Bagtzoglou A (2016) Streptococcus oralis and Candida albicans synergistically activate μ-calpain to degrade e-cadherin from oral epithelial junctions. J Infect Dis 214(6):925–934. https://doi.org/10.1093/infdis/jiw201CrossRefPubMedPubMedCentral

11.

Sanchez-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.2013.06.006CrossRefPubMed

12.

Falsetta ML, Klein MI, Colonne PM, Scott-Anne K, Gregoire S, Pai C-H, Gonzalez-Begne M, Watson G, Krysan DJ, Bowen WH, Koo H (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.00087-14CrossRefPubMedPubMedCentral

13.

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.2019.105815CrossRefPubMed

14.

Nikawa H, Egusa H, Makihira S, Yamashiro H, Fukushima H, Jin C, Nishimura M, Pudji RR, Hamada T (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.xCrossRefPubMed

15.

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.xCrossRefPubMed

16.

Paranhos HF, Silva-Lovato CH, Souza RF, Cruz PC, Freitas KM, Peracini A (2007) Effects of mechanical and chemical methods on denture biofilm accumulation. J Oral Rehabil 34(8):606–612. https://doi.org/10.1111/j.1365-2842.2007.01753.xCrossRefPubMed

17.

Jagger DC, Harrison A (1995) Denture cleansing–the best approach. Br Dent J 178(11):413–417CrossRef

18.

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.2016.089CrossRefPubMedPubMedCentral

19.

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.2014.07.004CrossRefPubMed

20.

Carrera ET, Dias HB, Corbi SCT, Marcantonio RAC, Bernardi ACA, Bagnato VS, Hamblin MR, Rastelli ANS (2016) The application of antimicrobial photodynamic therapy (aPDT) in dentistry: a critical review. Laser Phys 26 (12). https://doi.org/10.1088/1054-660x/26/12/123001

21.

Abegg MA, Alabarse PV, Casanova A, Hoscheid J, Salomon TB, Hackenhaar FS, Medeiros TM, Benfato MS (2010) Response to oxidative stress in eight pathogenic yeast species of the genus Candida. Mycopathologia 170(1):11–20. https://doi.org/10.1007/s11046-010-9294-5CrossRefPubMed

22.

Imamura T, Tatehara S, Takebe Y, Tokuyama R, Ohshima T, Maeda N, Satomura K (2014) Antibacterial and antifungal effect of 405 nm monochromatic laser on endodontopathogenic microorganisms. Int J Photoenergy 2014:1–7. https://doi.org/10.1155/2014/387215CrossRef

23.

Terada C, Imamura T, Ohshima T, Maeda N, Tatehara S, Tokuyama-Toda R, Yamachika S, Toyoda N, Satomura K (2018) The effect of irradiation with a 405 nm blue-violet laser on the bacterial adhesion on the osteosynthetic biomaterials. Int J Photoenergy 2018:1–10. https://doi.org/10.1155/2018/2635964CrossRef

24.

Plavskii VY, Mikulich AV, Tretyakova AI, Leusenka IA, Plavskaya LG, Kazyuchits OA, Dobysh II, Krasnenkova TP (2018) Porphyrins and flavins as endogenous acceptors of optical radiation of blue spectral region determining photoinactivation of microbial cells. J Photochem Photobiol B 183:172–183. https://doi.org/10.1016/j.jphotobiol.2018.04.021CrossRefPubMed

25.

Tsutsumi-Arai C, Arai Y, Terada-Ito C, Takebe Y, Ide S, Umeki H, Tatehara S, Tokuyama-Toda R, Wakabayashi N, Satomura K (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/s10103-019-02751-2CrossRefPubMed

26.

Gomez GF, Huang R, MacPherson M, Ferreira Zandona AG, Gregory RL (2016) Photo inactivation of streptococcus mutans biofilm by violet-blue light. Curr Microbiol 73(3):426–433. https://doi.org/10.1007/s00284-016-1075-zCrossRefPubMed

27.

Kadowaki O, Ogasawara A, Watanabe T, Mikami T, Matsumoto T, Misawa Y, Matahira Y, Sakai K (2007) Chitohexose induce the yeast proliferation of Candida albicans. Biol Pharm Bull 30(3):583–584. https://doi.org/10.1248/bpb.30.583CrossRefPubMed

28.

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.2015.11.010CrossRefPubMed

29.

Ota U, Fukuhara H, Ishizuka M, Abe F, Kawada C, Tamura K, Tanaka T, Inoue K, Ogura SI, Shuin T (2015) Plasma protoporphyrin IX following administration of 5-aminolevulinic acid as a potential tumor marker. Mol Clin Oncol 3(4):797–801. https://doi.org/10.3892/mco.2015.549CrossRefPubMedPubMedCentral

30.

Tsutsumi-Arai C, Takakusaki K, Arai Y, Terada-Ito C, Takebe Y, Imamura T, Ide S, Tatehara S, Tokuyama-Toda R, Wakabayashi N, Satomura K (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.0217496CrossRefPubMedPubMedCentral

31.

Misba L, Zaidi S, Khan AU (2018) Efficacy of photodynamic therapy against Streptococcus mutans biofilm: Role of singlet oxygen. J Photochem Photobiol B 183:16–21. https://doi.org/10.1016/j.jphotobiol.2018.04.024CrossRefPubMed

32.

Zoric N, Kosalec I, Tomic S, Bobnjaric I, Jug M, Vlainic T, Vlainic J (2017) Membrane of Candida albicans as a target of berberine. BMC Complement Altern Med 17(1):268. https://doi.org/10.1186/s12906-017-1773-5CrossRefPubMedPubMedCentral

33.

Joniová J, Gerelli E, Zellweger M, Wagnières G (2016) Optimization and characterization of the endogenous production of protoporphyrin IX in a yeast model. J Biomed Opt 21(12):125008. https://doi.org/10.1117/1.jbo.21.12.125008CrossRefPubMed

34.

Walter AB, Simpson J, Jenkins JL, Skaar EP, Jansen ED (2020) Optimization of optical parameters for improved photodynamic therapy of Staphylococcus aureus using endogenous coproporphyrin III. Photodiagnosis Photodyn Ther 29:101624. https://doi.org/10.1016/j.pdpdt.2019.101624CrossRefPubMed

35.

Hoenes K, Hess M, Vatter P, Spellerberg B, Hessling M (2018) 405 nm and 450 nm Photoinactivation of Saccharomyces cerevisiae. Eur J Microbiol Immunol (Bp) 8(4):142–148. https://doi.org/10.1556/1886.2018.00023CrossRef

36.

Kalyanaraman B, Darley-Usmar V, Davies KJ, Dennery PA, Forman HJ, Grisham MB, Mann GE, Moore K, Roberts LJ 2nd, Ischiropoulos H (2012) Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 52(1):1–6. https://doi.org/10.1016/j.freeradbiomed.2011.09.030CrossRefPubMed

37.

Rastogi RP, Singh SP, Häder DP, Sinha RP (2010) Detection of reactive oxygen species (ROS) by the oxidant-sensing probe 2’,7’-dichlorodihydrofluorescein diacetate in the cyanobacterium Anabaena variabilis PCC 7937. Biochem Biophys Res Commun 397(3):603–607. https://doi.org/10.1016/j.bbrc.2010.06.006CrossRefPubMed

38.

Opydo-Chanek M, Śladowska K, Blicharski K, Mikeš J, Fedoročko P, Niemeyer U, Mazur L (2017) Comparison of in vitro antileukemic activity of 4-Hydroperoxyifosfamide and 4-Hydroperoxycyclophosphamide. Anticancer Res 37(11):6355–6361. https://doi.org/10.21873/anticanres.12088CrossRefPubMed

39.

Wang J, Xu W, Yang Z, Yan Y, Xie X, Qu N, Wang Y, Wang C, Hua J (2018) New diketopyrrolopyrrole-based ratiometric fluorescent probe for intracellular esterase detection and discrimination of live and dead cells in different fluorescence channels. ACS Appl Mater Interfaces 10(37):31088–31095. https://doi.org/10.1021/acsami.8b11365CrossRefPubMed

40.

Engel AS, Kranz HT, Schneider M, Tietze JP, Piwowarcyk A, Kuzius T, Arnold W, Naumova EA (2020) Biofilm formation on different dental restorative materials in the oral cavity. BMC Oral Health 20(1):162. https://doi.org/10.1186/s12903-020-01147-xCrossRefPubMedPubMedCentral

41.

Shemesh M, Tam A, Steinberg D (2007) Differential gene expression profiling of Streptococcus mutans cultured under biofilm and planktonic conditions. Microbiology (Reading) 153(Pt 5):1307–1317. https://doi.org/10.1099/mic.0.2006/002030-0CrossRef

42.

Takahashi N, Iwasa F, Inoue Y, Morisaki H, Ishihara K, Baba K (2014) Evaluation of the durability and antiadhesive action of 2-methacryloyloxyethyl phosphorylcholine grafting on an acrylic resin denture base material. J Prosthet Dent 112(2):194–203. https://doi.org/10.1016/j.prosdent.2013.08.020CrossRefPubMed

43.

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)00026-2CrossRefPubMed

44.

Leonhard M, Zatorska B, Moser D, Schneider-Stickler B (2019) Growth media for mixed multispecies oropharyngeal biofilm compositions on silicone. Biomed Res Int 2019:8051270. https://doi.org/10.1155/2019/8051270CrossRefPubMedPubMedCentral

45.

Gulati M, Nobile CJ (2016) Candida albicans biofilms: development, regulation, and molecular mechanisms. Microbes Infect 18(5):310–321. https://doi.org/10.1016/j.micinf.2016.01.002CrossRefPubMedPubMedCentral

46.

Kim D, Sengupta A, Niepa TH, Lee BH, Weljie A, Freitas-Blanco VS, Murata RM, Stebe KJ, Lee D, Koo H (2017) Candida albicans stimulates Streptococcus mutans microcolony development via cross-kingdom biofilm-derived metabolites. Sci Rep 7:41332. https://doi.org/10.1038/srep41332CrossRefPubMedPubMedCentral

47.

Sztajer H, Szafranski SP, Tomasch J, Reck M, Nimtz M, Rohde M, Wagner-Döbler I (2014) Cross-feeding and interkingdom communication in dual-species biofilms of Streptococcus mutans and Candida albicans. ISME J 8(11):2256–2271. https://doi.org/10.1038/ismej.2014.73CrossRefPubMedPubMedCentral

48.

Radford DR, Radford JR (1993) A SEM study of denture plaque and oral mucosa of denture-related stomatitis. J Dent 21(2):87–93. https://doi.org/10.1016/0300-5712(93)90151-fCrossRefPubMed

Title: Microbicidal effect of 405-nm blue LED light on Candida albicans and Streptococcus mutans dual-species biofilms on denture base resin
Authors: Chiaki Tsutsumi-Arai
Yuki Arai
Chika Terada-Ito
Takahiro Imamura
Seiko Tatehara
Shinji Ide
Noriyuki Wakabayashi
Kazuhito Satomura
Publication date: 01-03-2022
Publisher: Springer London
Keywords: Candida Balanitis
Candida Albicans
Denture
Streptococci
Published in: Lasers in Medical Science / Issue 2/2022
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-021-03323-z

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Microbicidal effect of 405-nm blue LED light on Candida albicans and Streptococcus mutans dual-species biofilms on denture base resin

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

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