Skip to main content

Advertisement

SpringerLink
Log in

Comparison of the effect of rose bengal- and eosin Y-mediated photodynamic inactivation on planktonic cells and biofilms of Candida albicans

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

Abstract

Candida albicans is an opportunistic yeast that can cause oral candidosis through the formation of a biofilm, an important virulence factor that compromises the action of antifungal agents. The objective of this study was to compare the effect of rose bengal (RB)- and eosin Y (EY)-mediated photodynamic inactivation (PDI) using a green light-emitting diode (LED; 532 ± 10 nm) on planktonic cells and biofilms of C. albicans (ATCC 18804). Planktonic cultures were treated with photosensitizers at concentrations ranging from 0.78 to 400 μM, and biofilms were treated with 200 μM of photosensitizers. The number of colony-forming unit per milliliter (CFU/mL) was compared by analysis of variance and Tukey's test (P ≤ 0.05). After treatment, one biofilm specimen of the control and PDI groups were examined by scanning electron microscopy. The photosensitizers (6.25, 25, 50, 200, and 400 μM of EY, and 6.25 μM of RB or higher) significantly reduced the number of CFU/mL in the PDI groups when compared to the control group. With respect to biofilm formation, RB- and EY-mediated PDI promoted reductions of 0.22 log10 and 0.45 log10, respectively. Scanning electron microscopy showed that the two photosensitizers reduced fungal structures. In conclusion, EY- and RB-mediated PDI using LED irradiation significantly reduced C. albicans planktonic cells and biofilms.

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
Fig. 5

Similar content being viewed by others

References

  1. Parahitiyawa NB, Samaranayake YH, Samaranayake LP, Ye J, Tsang PWK, Cheung BPK et al (2009) Interspecies variation in Candida biofilm formation studied using the Calgary biofilm device. APMIS 114:298–306. doi:10.1111/j.1600-0463.2006.apm_394.x

    Article  Google Scholar 

  2. Wilson D, Thewes S, Zakikhany K, Fradin C, Albrecht A, Almeida R. et al. (2009) Identifying infection-associated genes of Candida albicans in the postgenomic era. FEMS Yeast Res 1–13. doi: 10.1111/j.1567-1364.2009.00524.x

  3. Coogan MM, Fidel PL Jr, Komesu MC, Maeda N, Samaranayake LP (2006) Candida and mycotic infections. Adv Dent Res 19:130–138. doi:10.1177/154407370601900124

    Article  CAS  PubMed  Google Scholar 

  4. Samaranayake YH, Samaranayake LP (2001) Experimental oral candidiasis in animal models. Clin Microbiol Rev 14(2):398–429. doi:10.1128/CMR.14.2.398-429.2001

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Gaitan-Cepeda LA, Martinez-Gonzalez M, Ceballos-Salobrena A (2005) Oral candidosis as a clinical marker of immune failure in patients with HIV/AIDS on HAART. AIDS Patient Care STDs 19(2):70–77. doi:10.1089/apc.2005.19.70

    Article  PubMed  Google Scholar 

  6. Sanchez-Vargas LO, Ortiz-Lopes NG, Villar M, Moragues MD, Aguirre JM, Cashat Cruz M et al (2005) Point prevalence, microbiology and antifungal susceptibility patterns of oral Candida isolates colonizing or infecting Mexican HIV/AIDS patients and healthy persons. Rev Iberoam Micol 22(2):83–92. doi:10.1128/JCM.43.8.4159-4162.2005

    Article  PubMed  Google Scholar 

  7. Delgado ACD, Pedro RJ, Aoki FH, Resende MR, Trapasso P, Colombo AL et al (2009) Clinical and microbiological assessment of patients with a long-term diagnosis of human immunodeficiency virus infection and Candida oral colonization. Clin Microbiol Infect 15(4):364–71

    Article  CAS  PubMed  Google Scholar 

  8. Seneviratne CJ, Jin L, Samaranayake LP (2008) Biofilm lifestyle of Candida: a mini review. Oral Dis 14:582–590. doi:10.1111/j.1601-0825.2007.01424.x

    Article  CAS  PubMed  Google Scholar 

  9. Dunne WN (2003) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15:155–166. doi:10.1128/CMR.15.2.155-166.2002

    Article  Google Scholar 

  10. Vazquez JA (2010) Invasive fungal infections in the invasive care unit. Semin Respir Crit Care Med 31:79–86. doi:10.1055/s-0029-1246289

    Article  PubMed  Google Scholar 

  11. Souza SC, Junqueira JC, Balducci I, Ito-Koga CY, Munin E, Jorge AOC (2006) Photosensitization of different Candida species by low power laser light. Photochem Photobiol B Biol 83:34–38. doi:10.1016/j.jphotobiol.2005.12.002

    Article  Google Scholar 

  12. Souza RC, Junqueira JC, Rossoni RD, Pereira CA, Munin E, Jorge AOC (2010) Comparison of the photodynamic fungicidal efficacy of methylene blue, toluidine blue, malachite green and low-power laser irradiation alone against Candida albicans. Lasers Med Sci 25:385–389. doi:10.1007/s10103-009-0706-z

    Article  PubMed  Google Scholar 

  13. Konopka K, Goslinski T (2007) Photodynamic therapy in dentistry. J Dent Res 86:694–707. doi:10.1177/154405910708600803

    Article  CAS  PubMed  Google Scholar 

  14. Pleatzer K, Krammer B, Berlanda J, Berr F, Kiesslich T (2009) Photophysics and photochemistry of photodynamic therapy: fundamental aspects. Lasers Med Sci 24:259–268. doi:10.1007/s10103-008-0539-1

    Article  Google Scholar 

  15. Meisel P, Kocher T (2005) Photodynamic therapy for periodontal diseases: state of the art. J Photochem Photobiol B Biol 79:159–170. doi:10.1016/j.jphotobiol.2004.11.023

    Article  CAS  Google Scholar 

  16. Peloi LS, Soares RRS, Biondo CEG, Souza VR, Hioka N, Kimura E (2008) Photodynamic effect of light emitting-diode light on cell growth inhibition induced by methylene blue. J Biosci 33(2):231–237. doi:10.1007/s12038-008-0040-9

    Article  CAS  PubMed  Google Scholar 

  17. Soares BM, Silva DL, Sousa GR, Amorim JCF, Resende MA, Pinotti M, Cisalpino PS (2009) In vitro photodynamic inactivation of Candida spp. growth and adhesion to buccal epithelial cells. Photochem Photobiol B Biol 94:65–70. doi:10.1016/j.jphotobiol.2008.07.013

    Article  CAS  Google Scholar 

  18. Wainwright M (1998) Photodynamic antimicrobial chemotherapy (PACT). J Antimicrob Chemother 42:13–28. doi:10.1093/jac/42.1.13

    Article  CAS  PubMed  Google Scholar 

  19. Encinas MV, Rufs AM, Bertolotti SG, Previtali CM (2009) Xanthene dyes/amine as photoinitiators of radical polymerization: a comparative and photochemical study in aqueous medium. Polymer 50(13):2762–2767

    Article  CAS  Google Scholar 

  20. Paulino TP, Magalhaes PP, Thedei G Jr, Tedesco AC, Ciancaglini P (2005) Use of visible light-based photodynamic therapy to bacterial photoinactivation. Biochem Mol Biol Educ 33:46–49. doi:10.1002/bmb.2005.494033010424

    Article  CAS  PubMed  Google Scholar 

  21. Seneviratne CJ, Jin L, Samaranayake LP (2008) Biofilm lifestyle of Candida: a mini review. Oral Dis 14(7):582–90. doi:10.1111/j.1601-0825.2007.01424.x

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  23. Usacheva MN, Teichert MC, Biel MA (2003) The role of the methylene blue and toluidine blue monomers and dimers in the photoinactivation of bacteria. J Photochem Photobiol B 71(1–3):87–98

    Article  CAS  PubMed  Google Scholar 

  24. Demidova TN, Hamblin MR (2005) Effect of cell-photosensitizer binding and cell density on microbial photoinactivation. Antimicrob Agents Chemother 49(6):2329–2335. doi:10.1128/AAC.49.6.2329-2335.2005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Dovigo LN, Pavarina AC, Mima EGO, Giampaolo ET, Vergani CE, Bagnato VS (2011) Fungicidal effect of photodynamic therapy against fluconazole-resistant Candida albicans and Candida glabrata. Mycoses 54(2):123–130. doi:10.1111/j.1439-0507.2009.01769.x

    Article  CAS  PubMed  Google Scholar 

  26. Nobile CJ, Mitchell AP (2006) Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol 8(9):1382–91. doi:10.1111/j.1462-5822.2006.00761.x

    Article  CAS  PubMed  Google Scholar 

  27. Ramage G, Walle KV, Wickes BL, Lopes-Ribot JL (2001) Biofilm formation by Candida dubliniensis. J Clin Microbiol 39(9):3234–40. doi:10.1128/JCM.39.9.3234-3240.2001

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Costa ACBP, Rasteiro VMC, Pereira CA, Rossoni RD, Junqueira JC, Jorge AOC (2012) The effects of rose bengal and erythrosine mediated photodynamic therapy on Candida albicans. Mycoses 55(1):56–63. doi:10.1111/j.1439-0507.2011.02042.x

    Article  CAS  PubMed  Google Scholar 

  29. Seneviratne CJ, Silva WJ, Jin LJ, Samaranayake YH, Samaranayake LP (2009) Architectural analysis, viability assessment and growth kinetics of Candida albicans and Candida glabrata biofilms. Arch Oral Biol 54(11):1052–60. doi:10.1016/j.archoralbio.2009.08.002

    Article  CAS  PubMed  Google Scholar 

  30. Pereira CA, Romeiro RL, Costa ACBP, Machado AKS, Junqueira JC, Jorge AO (2011) Susceptibility of Candida albicans, Staphylococcus aureus, and Streptococcus mutans biofilms to photodynamic inactivation: an in vitro study. Lasers Med Sci May 26(3):341–8. doi:10.1007/s10103-010-0852-3

    Article  Google Scholar 

  31. Costa ACBP, Rasteiro VMC, Pereira CA, Hashimoto ESHS, Junior MB, Junqueira JC, Jorge AOC (2011) Susceptibility of Candida albicans and Candida dubliniensis to erythrosine- and LED-mediated photodynamic therapy. Arch Oral Biol 56:1299–1305. doi:10.1016/j.archoralbio.2011.05.013

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Brazil (grant 2009/52048-1). The authors Fernanda Freire, Cristiane A. Pereira, and Anna Carolina B. P. Costa are grateful to FAPESP for the provided scholarships (Processes 2010/12115-9, 2010/00879-4, and 2011/21346-7).

Author information

Authors and Affiliations

  1. Department of Biosciences and Oral Diagnosis, Institute of Science and Technology, UNESP - Universidade Estadual Paulista, Francisco José Longo 777, São Dimas, São José dos Campos, 12245-000, São Paulo, Brazil

    Fernanda Freire, Anna Carolina Borges Pereira Costa, Cristiane Aparecida Pereira, Juliana Campos Junqueira & Antonio Olavo Cardoso Jorge

  2. Institute of Research and Development (IP&D), Universidade do Vale do Paraíba - UNIVAP, Shishima Hifumi, 2911, Urbanova, São José dos Campos, 12244-000, São Paulo, Brazil

    Milton Beltrame Junior

Authors
  1. Fernanda Freire
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Carolina Borges Pereira Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cristiane Aparecida Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Milton Beltrame Junior
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juliana Campos Junqueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Antonio Olavo Cardoso Jorge
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernanda Freire.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Freire, F., Costa, A.C.B.P., Pereira, C.A. et al. Comparison of the effect of rose bengal- and eosin Y-mediated photodynamic inactivation on planktonic cells and biofilms of Candida albicans . Lasers Med Sci 29, 949–955 (2014). https://doi.org/10.1007/s10103-013-1435-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-013-1435-x

Keywords

Search

Navigation