Advertisement

Lasers in Medical Science

, Volume 30, Issue 9, pp 2303–2312 | Cite as

Photodynamic inactivation of a multispecies biofilm using Photodithazine® and LED light after one and three successive applications

  • Cristiane Campos Costa Quishida
  • Ewerton Garcia de Oliveira Mima
  • Lívia Nordi Dovigo
  • Janaina Habib Jorge
  • Vanderlei Salvador Bagnato
  • Ana Cláudia Pavarina
Original Article

Abstract

In this investigation, the effectiveness of successive applications of antimicrobial photodynamic inactivation (API) mediated by Photodithazine® (PDZ) and LED light was evaluated against a multispecies biofilm formed by Candida albicans, Candida glabrata, and Streptococcus mutans on denture base acrylic resin. Standard cell suspensions (bacteria and yeast) were inoculated on acrylic resin samples, and the biofilm was grown for 48 h (37 °C/75 rpm). API was performed by the administration of PDZ (175 and 200 mg/L) and exposure to 37.5 J/cm2 of LED light (660 nm). Additional samples were treated with PDZ or LED light only. Untreated control samples were not submitted to light or PDZ. The conditions described were applied once or in three consecutive applications for all groups. Cell viability was determined by colony counts (CFU/mL), metabolic activity, total biomass, and confocal laser scanning microscopy (CLSM). Data were analyzed by a nonparametric two-way ANOVA and Tukey tests (α = 0.05). The results obtained demonstrated a significant effect (p < 0.05) of number of applications and treatment groups for CFU/mL, and S. mutans showed the highest susceptibility to API. The metabolic activity of the multispecies biofilm was significantly reduced (p < 0.05) after API for both numbers of applications, which were also significantly different (p < 0.05) between them. The total biomass of the biofilm was significantly different (p < 0.05) only between groups submitted to one and three API applications. CLSM showed a visual increase of dead cells after API. API-mediated PDZ was effective in reducing the cell viability of multispecies biofilm. Three consecutive applications of API were more effective for reducing the cell viability and the total biomass of multispecies biofilm.

Keywords

Biofilm Candida albicans Candida glabrata Streptococcus mutans Acrylic resin Photodynamic therapy 

Notes

Acknowledgments

This work was supported by the São Paulo Research Foundation—FAPESP (grant 2011/09054), Centro de Pesquisa em Óptica e Fotônica—CEPOF-CEPID (grant 13/07276-1), and Fundação para o Desenvolvimento da UNESP—FUNDUNESP (grant 878/11-DFP).

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Akpan A, Morgan R (2002) Oral candidiasis. Postgrad Med J 78:455–9PubMedCentralCrossRefPubMedGoogle Scholar
  2. 2.
    Gendreau L, Loewy ZG (2011) Epidemiology and etiology of denture stomatitis. J Prosthodont 20:251–60CrossRefPubMedGoogle Scholar
  3. 3.
    Ramage G, Vandewalle K, Wickes BL, Lopez-Ribot JL (2001) Characteristics of biofilm formation by Candida albicans. Rev Iberoam Micol 18(4):163–170PubMedGoogle Scholar
  4. 4.
    Lamfon H, Al-Karaawi Z, McCullough M, Porter SR, Pratten J (2005) Composition of in vitro denture plaque biofilms and susceptibility to antifungals. FEMS Microbiol Lett 242:345–51CrossRefPubMedGoogle Scholar
  5. 5.
    Baena-Monroy T, Moreno-Maldonado V, Franco-Martínez F, Aldape-Barrios B, Quindós G, Sánchez-Vargas LO (2005) Candida albicans, Staphylococcus aureus and Streptococcus mutans colonization in patients wearing dental prosthesis. Med Oral Patol Oral Cir Bucal 10:27–39Google Scholar
  6. 6.
    Ribeiro DG, Pavarina AC, Dovigo LN, Spolidorio DMP, Giampaolo ET, Vergani CE (2009) Denture disinfection by microwave irradiation: a randomized clinical study. J Dent 37:666–72CrossRefPubMedGoogle Scholar
  7. 7.
    Neppelenbroek KH, Pavarina AC, Spolidorio DMP, Sgavioli Massucato EM, Spolidorio LC, Vergani CE (2008) Effectiveness of microwave disinfection of complete dentures on the treatment of Candida-related denture stomatitis. J Oral Rehabil 35:836–46CrossRefPubMedGoogle Scholar
  8. 8.
    Mima EG, Vergani CE, Machado AL, Massucato EM, Colombo AL, Bagnato VS et al (2012) Comparison of Photodynamic Therapy versus conventional antifungal therapy for the treatment of denture stomatitis: a randomized clinical trial. Clin Microbiol Infect 18:E380–8CrossRefPubMedGoogle Scholar
  9. 9.
    Budtz-Jorgensen E, Theilade E (1983) Regional variations in viable bacterial and yeast counts of 1-week-old denture plaque in denture-induced stomatitis. Scand J Dent Res 91:288–95PubMedGoogle Scholar
  10. 10.
    Theilade E, Budtz-Jorgensen E (1988) Predominant cultivable microflora of plaque on removable dentures in patients with denture-induced stomatitis. Oral Microbiol Immunol 3:8–13CrossRefPubMedGoogle Scholar
  11. 11.
    Jeganathan S, Lin CC (1992) Denture stomatitis—a review of the aetiology, diagnosis and management. Aust Dent J 37:107–114CrossRefPubMedGoogle Scholar
  12. 12.
    Pereira-Cenci T, Deng DM, Kraneveld EA, Manders EM, Del Bel Cury AA, Ten Cate JM et al (2008) The effect of Streptococcus mutans and Candida glabrata on Candida albicans biofilms formed on different surfaces. Arch Oral Biol 53:755–64CrossRefPubMedGoogle Scholar
  13. 13.
    Martin MV (1999) The use of fluconazole and itraconazole in the treatment of Candida albicans infections: a review. J Antimicrob Chemother 44:429–37CrossRefPubMedGoogle Scholar
  14. 14.
    Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183:5385–5394PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    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):203–205Google Scholar
  16. 16.
    Hunter KD, Gibson J, Lockhart P, Pithie A, Bagg J (1999) Fluconazole resistant Candida species in the oral flora of fluconazole-exposed HIV-positive patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 85:558–564CrossRefGoogle Scholar
  17. 17.
    White TC, Marr KA, Bowden RA (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11:382–402PubMedCentralPubMedGoogle Scholar
  18. 18.
    Zanin IC, Gonçalves RB, Junior AB, Hope CK, Pratten J (2005) Susceptibility of Streptococcus mutans biofilms to photodynamic therapy: an in vitro study. J Antimicrob Chemother 56:324–30CrossRefPubMedGoogle Scholar
  19. 19.
    Goulart RC, Bolean M, Paulino TP, Thedei G Jr, Souza SL, Tedesco AC et al (2010) Photodynamic therapy in planktonic and biofilm cultures of Aggregatibacter actinomycetemcomitans. Photomed Laser Surg 28:S53–60CrossRefGoogle Scholar
  20. 20.
    Dovigo LN, Pavarina AC, Mima EG, Giampaolo ET, Vergani CE, Bagnato VS (2011) Fungicidal effect of photodynamic therapy against fluconazole-resistant Candida albicans and Candida glabrata. Mycoses 54:123–30CrossRefPubMedGoogle Scholar
  21. 21.
    Mima EG, Pavarina AC, Ribeiro DG, Dovigo LN, Vergani CE, Bagnato VS (2011) Effectiveness of photodynamic therapy for the inactivation of Candida spp. on dentures: in vitro study. Photomed Laser Surg 29:827–33PubMedCentralCrossRefPubMedGoogle Scholar
  22. 22.
    Andrade MC, Ribeiro AP, Dovigo LN, Brunetti IL, Giampaolo ET, Bagnato VS et al (2013) Effect of different pre-irradiation times on curcumin-mediated photodynamic therapy against planktonic cultures and biofilms of Candida spp. Arch Oral Biol 58:200–10CrossRefPubMedGoogle Scholar
  23. 23.
    Pereira CA, Romeiro RL, Costa AC, Machado AK, 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 26:341–8CrossRefPubMedGoogle Scholar
  24. 24.
    Donnelly RF, McCarron PA, Tunney MM (2008) Antifungal photodynamic therapy. Microbiol Res 163:1–12CrossRefPubMedGoogle Scholar
  25. 25.
    Correa JC, Bagnato VS, Imasato H, Perussi JR (2012) Previous illumination of a water soluble chlorine photosensitizer increases its cytotoxicity. Laser Phys 22:1387–94CrossRefGoogle Scholar
  26. 26.
    Ferreira J, Menezes PFC, Kurachi C, Sibata C, Allison RR, Bagnato VS (2008) Photostability of different chlorine photossensitizers. Laser Phys Lett 5:156–61CrossRefGoogle Scholar
  27. 27.
    Park JH, Moon YH, Bang IS, Kim YC, Kim SA, Ahn SG et al (2010) Antimicrobial effect of photodynamic therapy using a highly pure chlorine e6. Laser Med Sci 25:705–10CrossRefGoogle Scholar
  28. 28.
    Strackhovskaya MG, Belenikina NS, Ivanova EV, Chemeris YK, Stranadko EF (2002) The photodynamic inactivation of the yeast Candida guilliermondii in the presence of photodithazine. Microbiol 71:345–48Google Scholar
  29. 29.
    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 Sci22:804.Google Scholar
  30. 30.
    Fekrazad R, Khoei F, Hakimiha N, Bahador A. Photoelimination of Streptococcus mutans with two methods of photodynamic and photothermal therapy. Photodiagnosis Photodyn Ther. Dec;10(4):62631Google Scholar
  31. 31.
    Fekrazad R, Bargrizan M, Sajadi S, Sajadi S (2013) Evaluation of the effect of photoactivated disinfection with Radachlorin(®) against Streptococcus mutans (an in vitro study). Photodiagnosis Photodyn Ther 8:24953Google Scholar
  32. 32.
    Dovigo LN, Carmello JC, Carvalho MT, Mima EG, Vergani CE, Bagnato VS et al (2013) Photodynamic inactivation of clinical isolates of Candida using Photodithazine®. Biofouling 29:1057–67CrossRefPubMedGoogle Scholar
  33. 33.
    Quishida CC, Carmello JC, Mima EG, Bagnato VS, Machado AL, Pavarina AC (2015) Susceptibility of multispecies biofilm to photodynamic therapy using Photodithazine®. Lasers Med Sci 30:685–94CrossRefPubMedGoogle Scholar
  34. 34.
    Dovigo LN, Pavarina AC, Carmello JC, Machado AL, Brunetti IL, Bagnato VS (2011) Susceptibility of clinical isolates of Candida to photodynamic effects of curcumin. Lasers Surg Med 43:927–34CrossRefPubMedGoogle Scholar
  35. 35.
    Mima EG, Pavarina AC, Silva MM, Ribeiro DG, Vergani CE, Kurachi C, Bagnato VS (2011) Denture stomatitis treated with photodynamic therapy: five cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 112:602–8CrossRefPubMedGoogle Scholar
  36. 36.
    Zissis AJ, Polyzois GL, Yannikakis SA, Harrison A (2000) Roughness of denture materials: a comparative study. Int J Prosthodont 13:136–40PubMedGoogle Scholar
  37. 37.
    Millsap KW, Bos R, van der Mei HC, Busscher HJ (1999) Adhesion and surface-aggregation of Candida albicans from saliva on acrylic surfaces with adhering bacteria as studied in a parallel plate flow chamber. Antonie Van Leeuwenhoek 75:351–9CrossRefPubMedGoogle Scholar
  38. 38.
    Chandra J, Mukherjee PK, Leidich SD, Faddoul FF, Hoyer LL, Douglas LJ et al (2001) Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J Dent Res 80:903–8CrossRefPubMedGoogle Scholar
  39. 39.
    Mima EG, Pavarina AC, Neppelenbroek KH, Vergani CE, Spolidorio DM, Machado AL (2008) Effect of different exposure times on microwave irradiation on the disinfection of a hard chairside reline resin. J Prosthodont 17:312–7CrossRefPubMedGoogle Scholar
  40. 40.
    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 54:1052–60CrossRefPubMedGoogle Scholar
  41. 41.
    Silva S, Henriques M, Martins A, Oliveira R, Williams D, Azeredo J (2009) Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. Med Mycol 47:681–689CrossRefPubMedGoogle Scholar
  42. 42.
    Mima EG, Pavarina AC, Dovigo LN, Vergani CE, Costa CA, Kurachi C, Bagnato VS (2010) Susceptibility of Candida albicans to photodynamic therapy in a murine model of oral candidosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 109:392–401CrossRefPubMedGoogle Scholar
  43. 43.
    Carmello JC, Dovigo LN, Mima EG, Jorge JH, de Souza Costa CA, Bagnato VS, Pavarina AC (2015) In vivo evaluation of photodynamic inactivation using Photodithazine® against Candida albicans. Photochem Photobiol Sci 14:1319–28CrossRefPubMedGoogle Scholar
  44. 44.
    Demidova TN, Hamblin MR (2005) Effect of cell-photosensitizer binding and cell density on microbial photoinactivation. Antimicrob Agents Chemother 49:2329–35PubMedCentralCrossRefPubMedGoogle Scholar
  45. 45.
    Paardekooper M, De Bruijne AW, Van Steveninck J, Van den Broek PJ (1995) Intracellular damage in yeast cells caused by photodynamic treatment with toluidine blue. Photochem Photobiol 61:84–9CrossRefPubMedGoogle Scholar
  46. 46.
    Khot PD, Suci PA, Tyler BJ (2008) Candida albicans viability after exposure to amphotericin B: assessment using metabolic assays and colony forming units. J Microbiol Methods 72:268–74CrossRefPubMedGoogle Scholar
  47. 47.
    Parahitiyawa NB, Samaranayake YH, Samaranayake LP, Ye J, Tsang PW, Cheung BP, Yau JY, Yeung SK (2006) Interspecies variation in Candida biofilm formation studied using the Calgary biofilm device. APMIS 114:298–306CrossRefPubMedGoogle Scholar
  48. 48.
    Thein ZM, Samaranayake YH, Samaranayake LP (2007) In vitro biofilm formation of Candida albicans and non-albicans Candida species under dynamic and anaerobic conditions. Arch Oral Biol 52:761–7CrossRefPubMedGoogle Scholar
  49. 49.
    Konopka K, Goslinski T (2007) Photodynamic therapy in dentistry. J Dent Res 86:694–707CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag London 2015

Authors and Affiliations

  • Cristiane Campos Costa Quishida
    • 1
  • Ewerton Garcia de Oliveira Mima
    • 1
  • Lívia Nordi Dovigo
    • 2
  • Janaina Habib Jorge
    • 1
  • Vanderlei Salvador Bagnato
    • 3
  • Ana Cláudia Pavarina
    • 1
  1. 1.Department of Dental Materials and Prosthodontics, Araraquara Dental SchoolUNESP, Univ Estadual PaulistaAraraquaraBrazil
  2. 2.Department of Social Dentistry, Araraquara Dental SchoolUNESP – Univ Estadual PaulistaAraraquaraBrazil
  3. 3.Physics Institute of São CarlosUSP, University of São PauloSão CarlosBrazil

Personalised recommendations