Skip to main content

Advertisement

SpringerLink
Log in

Twice-daily red and blue light treatment for Candida albicans biofilm matrix development control

  • Original Article
  • Published:
Lasers in Medical Science Aims and scope Submit manuscript

Abstract

Phototherapy has been proposed as a direct means of affecting local bacterial infections. However, the use of phototherapy to prevent fungal biofilm development has received comparatively less attention. This study aimed to determine the effects of red light treatment and blue light treatment, without a photosensitizer, on the development of Candida albicans biofilm. During the development of 48-h biofilms of C. albicans SN 425 (n = 10), the biofilms were exposed twice-daily to noncoherent blue and red light (LumaCare; 420 nm and 635 nm). The energy density applied was 72 J cm−2 for blue light and 43.8 J cm2, 87.6 J cm2, and 175.5 J cm2 for red light. Positive control (PC) and negative control (NC) groups were treated twice-daily for 1 min with 0.12% chlorhexidine (CHX) and 0.89% NaCl respectively. Biofilms were analyzed for colony forming units (CFU), dry-weight, and exopolysaccharides (EPS-soluble and EPS-insoluble). Data was analyzed by one-way ANOVA and Tukey post hoc test (α = 0.05). Dry-weight was lower than NC (p < 0.001) and approached PC levels with both red and blue light treatments. CFU were also lower in groups exposed to blue light and higher durations of red light (p < 0.05). EPS-soluble and EPS-insoluble measures were variably reduced by these light exposures. In conclusion, twice-daily exposure to both blue and red lights affect the biofilm development and physiology of polysaccharide production and are potential mechanisms for the control of C. albicans biofilm matrix development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Sardi JCO, Scorzoni L, Bernardi T, Fusco-Almeida AM, Mendes Giannini MJ (2013) Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol 62:10–24. https://doi.org/10.1099/jmm.0.045054-0

    Article  PubMed  CAS  Google Scholar 

  2. Harriott MM, Noverr MC (2009) Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 53:3914–3922. https://doi.org/10.1128/AAC.00657-09

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Sudbery PE (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9:737–748. https://doi.org/10.1038/nrmicro2636

    Article  PubMed  CAS  Google Scholar 

  4. 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 58:1318–1326. https://doi.org/10.1016/j.archoralbio.2013.06.006

    Article  PubMed  CAS  Google Scholar 

  5. Sutherland IW (2001) The biofilm matrix an immobilized but dynamic microbial environment. Trends Microbiol 9:222–227

    Article  PubMed  CAS  Google Scholar 

  6. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633. https://doi.org/10.1038/nrmicro2415

    Article  PubMed  CAS  Google Scholar 

  7. Williams DW, Kuriyama T, Silva S, Malic S, Lewis MA (2011) Candida biofilms and oral candidosis: treatment and prevention. Periodontol 55:250–265. https://doi.org/10.1111/j.1600-0757.2009.00338.x

    Article  Google Scholar 

  8. Zarnowski R, Westler WM, Lacmbouh GA et al (2014) Novel entries in a fungal biofilm matrix encyclopedia. MBio 5:e01333–e01314. https://doi.org/10.1128/mBio.01333-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Mitchell KF, Zarnowski R, Sanchez H et al (2015) Community participation in biofilm matrix assembly and function. Proc Natl Acad Sci U S A 112:4092–4097. https://doi.org/10.1073/pnas.1421437112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Mitchell KF, Zarnowski R, Andes DR (2016) Fungal super glue: the biofilm matrix and its composition, assembly, and functions. PLoS Pathog 12:e1005828. https://doi.org/10.1371/journal.ppat.1005828

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Xiao J, Koo H (2010) Structural organization and dynamics of exopolysaccharide matrix and microcolonies formation by Streptococcus mutans in biofilms. J Appl Microbiol 108:2103–2113. https://doi.org/10.1111/j.1365-2672.2009.04616.x

    Article  PubMed  CAS  Google Scholar 

  12. Paschoal MA, Lin M, Santos-Pinto L, Duarte S (2015) Photodynamic antimicrobial chemotherapy on Streptococcus mutans using curcumin and toluidine blue activated by a novel LED device. Lasers Med Sci 30:885–890. https://doi.org/10.1007/s10103-013-1492-1

    Article  PubMed  Google Scholar 

  13. Donnelly RF, MsCarron PA, Tunney MM (2008) Antifungal photodynamic therapy. Microbiol Res 163:1–12

    Article  PubMed  CAS  Google Scholar 

  14. Lins de Sousa D, Araujo RL, Zanin IC et al (2015) Effect of twice-daily blue light treatment on matrix-rich biofilm development. PLoS One 10:e0131941. https://doi.org/10.1371/journal.pone.0131941

    Article  PubMed Central  CAS  Google Scholar 

  15. Panariello BHD, Klein MI, Pavarina AC, Duarte S (2017) Inactivation of genes TEC1 and EFG1 in Candida albicans influences extracellular matrix composition and biofilm morphology. J Oral Microbiol 9(1):1385372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Koo H, Xiao J, Klein MI (2009) Extracellular polysaccharides matrix – an often forgotten virulence factor in oral biofilm research. Int J Oral Sci 1:229–234. https://doi.org/10.4248/IJOS.09086

    Article  PubMed  PubMed Central  Google Scholar 

  17. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  18. Banting DW, Greenhorn PA, McMinn JG (1995) Effectiveness of a topical antifungal regimen for the treatment of oral candidiasis in older, chronically ill, institutionalized, adults. J Can Dent Assoc 61(199–200):203–205

    Google Scholar 

  19. Samaranayake LP, Keung Leung W, Jin L (2009) Oral mucosal fungal infections. Periodontol 49:39–59. https://doi.org/10.1111/j.1600-0757.2008.00291.x

    Article  Google Scholar 

  20. Bliss JM, Bigelow CE, Foster TH, Haidaris CG (2004) Susceptibility of Candida species to photodynamic effects of Photofrin. Antimicrob Agents Chemother 48:2000–2006. https://doi.org/10.1128/AAC.48.6.2000-2006.2004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Dovigo LN, Pavarina AC, Mima EGO et al (2011) Fungicidal effect of photodynamic therapy against fluconazole-resistant Candida albicans and Candida glabrata. Mycoses 54:123–130. https://doi.org/10.1111/j.1439-0507.2009.01769.x

    Article  PubMed  CAS  Google Scholar 

  22. Mima EG, Pavarina AC, Dovigo LN et al (2012) Susceptibility of Candida albicans to photodynamic therapy in a murine model of oral candidosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 109:392–401. https://doi.org/10.1016/j.tripleo.2009.10.006

    Article  Google Scholar 

  23. Fontana CR, Abernethy AD, Som S et al (2009) The antibacterial effect of photodynamic therapy in dental plaque-derived biofilms. J Periodontal Res 44:751–759. https://doi.org/10.1111/j.1600-0765.2008.01187.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Al-Fattani MA, Douglas LJ (2006) Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55:999–1008. https://doi.org/10.1099/jmm.0.46569-0

    Article  PubMed  CAS  Google Scholar 

  25. Nett J, Andes D (2006) Candida albicans biofilm development, modeling a host-pathogen interaction. Curr Opin Microbiol 9:340–345. https://doi.org/10.1016/j.mib.2006.06.007

    Article  PubMed  CAS  Google Scholar 

  26. Nett J, Lincoln L, Marchillo K et al (2007) Putative role of β-1,3 glucans in Candida albicans biofilm resistance. Antimicrob Agents Chemother 51:510–520. https://doi.org/10.1128/AAC.01056-06

    Article  PubMed  CAS  Google Scholar 

  27. Vediyappan G, Rossignol T, d'Enfert C (2010) Interaction of Candida albicans biofilms with antifungals: transcriptional response and binding of antifungals to beta-glucans. Antimicrob Agents Chemother 54:2096–2111. https://doi.org/10.1128/AAC.01638-09

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Dovigo LN, Carmello JC, Carvalho MT, Mima EG, Vergani CE, Bagnato VS, Pavarina AC (2013) Photodynamic inactivation of clinical isolates of Candida using Photodithazine®. Biofouling 29:1057–1067

    Article  PubMed  CAS  Google Scholar 

  29. Quishida CC, Mima EG, Dovigo LN, Jorge JH, Bagnato VS, Pavarina AC (2015) Photodynamic inactivation of a multispecies biofilm using Photodithazine ® and LED light after one and three successive applications. Lasers Med Sci 30:2303–2312

    Article  PubMed  Google Scholar 

  30. Trigo Gutierrez JK, Zanatta GC, Ortega ALM, Balastegui MIC, Sanitá PV, Pavarina AC, Barbugli PA, MIMA EGO (2017) Encapsulation of curcumin in polymeric nanoparticles for antimicrobial photodynamic therapy. PLoS One 12:e0187418

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Duarte S, Kuo SP, Murata RM, Chen CY, Saxena D, Huang KJ, Popovic S (2011) Air plasma effect on dental disinfection. Phys Plasmas 18:Artn 073503. https://doi.org/10.1063/1.3606486

    Article  CAS  Google Scholar 

  32. Koban I, Holtfreter B, Hubner NO, Matthes R, Sietmann R, Kindel E, Weltmann KD, Welk A, Kramer A, Kocher T (2011) Antimicrobial efficacy of non-thermal plasma in comparison to chlorhexidine against dental biofilms on titanium discs in vitro - proof of principle experiment. J Clin Periodontol 38:956–965. https://doi.org/10.1111/j.1600-051X.2011.01740.x

    Article  PubMed  CAS  Google Scholar 

  33. Dai T (2017) The antimicrobial effect of blue light: what are behind? Virulence 8:649–652. https://doi.org/10.1080/21505594.2016.1276691

    Article  PubMed  PubMed Central  Google Scholar 

  34. Durantini EN (2016) New insights into the antimicrobial blue light inactivation of Candida albicans. Virulence 7:493–494. https://doi.org/10.1080/21505594.2016.1160194

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  36. Balagopal S, Arjunkumar R (2013) Chlorhexidine: the gold-standard antiplaque agent. J Pharm Sci Res 5:270–274

    Google Scholar 

  37. Mattos-Graner RO, Klein MI, Smith DJ (2014) Lessons learned from clinical studies: roles of Mutans streptococci in the pathogenesis of dental caries. Curr Oral Health Rep 1:70–78

    Article  Google Scholar 

  38. Zanatta FB, Antoniazzi RP, Rösing CK (2007) The effect of 0.12% chlorhexidine gluconate rinsing on previously plaque-free and plaque-covered surfaces: a randomized, controlled clinical trial. J Periodontol 78:2127–2134

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Alexander D. Johnson, Department of Microbiology and Immunology, UCSF, for his generous donation of the strain used in this study.

Funding

This research was supported by CAPES Foundation from whom the first author received a scholarship (CAPES 88881.062159̷ 2014-01 PVE̷ CAPES). The funder had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Department of Restorative Dentistry, Federal University of Ceará, Rua Monsenhor Furtado, s/n. Rodolfo Teófilo, Fortaleza, Ceará, 60430-355, Brazil

    Paula Ventura da Silveira, Cecília Atem Gonçalves de Araújo Costa & Iriana Carla Junqueira Zanin

  2. Department of Cariology, Operative Dentistry and Dental Public Health, Indiana University, Purdue University Indianapolis, School of Dentistry, Postal address: 1121 W Michigan St, # DS406, Indianapolis, IN, 46202, USA

    Beatriz Helena Dias Panariello & Simone Duarte

  3. New York University College of Dentistry, 345 E. 24th Street, New York, NY, 10010, USA

    Shawn M. Maule & Shane M. Maule

  4. Department of Epidemiology and Health Promotion, New York University College of Dentistry, 345 E. 24th Street, New York, NY, 10010, USA

    Malvin N. Janal

Authors
  1. Paula Ventura da Silveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Beatriz Helena Dias Panariello
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecília Atem Gonçalves de Araújo Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shawn M. Maule
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shane M. Maule
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Malvin N. Janal
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Iriana Carla Junqueira Zanin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Simone Duarte
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Simone Duarte.

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

The authors have attested that for this type of study, formal consent is not required.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silveira, P.V., Panariello, B.H.D., de Araújo Costa, C.A.G. et al. Twice-daily red and blue light treatment for Candida albicans biofilm matrix development control. Lasers Med Sci 34, 441–447 (2019). https://doi.org/10.1007/s10103-018-2610-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-018-2610-x

Keywords

Search

Navigation