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Effectiveness of antimicrobial photodynamic therapy with indocyanine green against the standard and fluconazole-resistant Candida albicans

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Abstract

Antimicrobial photodynamic therapy (aPDT) is an alternative approach. The current study aimed to investigate the efficacy of aPDT with indocyanine green (ICG) against two Candida albicans (C. albicans) strains. In this in vitro study, the inoculum of standard ATCC 10,231 (S) and fluconazole-resistant (FR) strains were adjusted to the turbidity of a 0.5 McFarland standard. Each strain was allocated into 4 groups: S1 and FR1) control groups, S2 and FR2) ICG-treated groups (1 µg/mL), S3 and FR3) laser-irradiated groups (wavelength: 810 nm; mode: continuous-wave; output power: 300 mW; spot size: 4.5 mm; exposure time: 120 s; radiation dose: 228 J/cm2), S4 and FR4) ICG-mediated-aPDT groups. After treatments, the number of colony-forming units per milliliter (CFU/mL) was calculated. Using the XTT reduction assay, the effects of each treatment on Candida biofilm formation were evaluated. Data were analyzed using SPSS software version 22. In both strains, the maximum number of CFUs was observed in the control group, followed by ICG-treated, laser-irradiated, and ICG-mediated-aPDT groups. In ATCC 10,231 strain, the XTT assay exhibited significant difference between ICG-mediated-aPDT and control groups (p < 0.0001). However, the ICG, laser, and ICG-mediated-aPDT groups in fluconazole-resistant strain showed significant differences when compared with the control (p < 0.05). The mean Candida CFUs and the XTT assay did not show any significant difference between the ATCC 10,231 and fluconazole-resistant strains with respect to each treatment. Data suggest ICG-mediated-aPDT could diminish Candida CFUs in laboratory; however, further studies are warranted to confirm its efficacy and safety to be applied in clinics.

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References

  1. Al-Sanabani NF, Al-Kebsi AM, Al-Shamahy HA, Abbas A-KM (2018) Etiology and risk factors of stomatitis among Yemeni denture wearers. Univers J Pharm Res 3(1):69–73

    Article  Google Scholar 

  2. Gendreau L, Loewy ZG (2011) Epidemiology and etiology of denture stomatitis. J Prosthodont 20(4):251–260

    Article  Google Scholar 

  3. Daliri F, Azizi A, Goudarzi M, Lawaf S, Rahimi A (2019) In vitro comparison of the effect of photodynamic therapy with curcumin and methylene blue on Candida albicans colonies. Photochem Photobiol Sci 26:193–198

    CAS  Google Scholar 

  4. Fekrazad R, Barghi VG, Poorsattar Bejeh Mir A, Shams-Ghahfarokhi M (2015) In vitro photodynamic inactivation of Candida albicans by phenothiazine dye (new methylene blue) and Indocyanine green (EmunDo®). Photochem Photobiol Sci 12(1):52–57

    CAS  Google Scholar 

  5. Patil S, Rao RS, Majumdar B, Anil S (2015) Clinical appearance of oral Candida infection and therapeutic strategies. Front Microbiol 6(1391):1–10

    Google Scholar 

  6. Afroozi B, Zomorodian K, Lavaee F, Shahrabadi ZZ, Mardani M (2019) Comparison of the efficacy of indocyanine green-mediated photodynamic therapy and nystatin therapy in treatment of denture stomatitis. Photochem Photobiol Sci 27(1):193–197

    CAS  Google Scholar 

  7. Allison RR, Moghissi K (2013) Photodynamic Therapy (PDT): PDT Mechanisms. Clin Endosc 46(1):24–29

    Article  Google Scholar 

  8. Rosa LP, da Silva FC (2014) Antimicrobial photodynamic therapy: a new therapeutic option to combat infections. J Med Microbiol 3(4):1–7

    Google Scholar 

  9. Andisheh-Tadbir A, Yaghoubi A, Tanideh N, Mardani M (2020) The effect of indocyanine green-mediated photodynamic therapy in healing of experimentally induced oral mucosal traumatic ulcer in rat. Lasers Med Sci 1–8

  10. Schaafsma BE, Mieog JSD, Hutteman M, Van der Vorst JR, Kuppen PJ, Löwik CW, Frangioni JV, Van de Velde CJ, Vahrmeijer AL (2011) The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery. J Surg Oncol 104(3):323–332

    Article  CAS  Google Scholar 

  11. Zelken JA, Tufaro AP (2015) Current trends and emerging future of indocyanine green usage in surgery and oncology: an update. Ann Surg Oncol 22(3):1271–1283

    Article  Google Scholar 

  12. Yannuzzi LA (2011) Indocyanine green angiography: a perspective on use in the clinical setting. Am J Ophthalmol 151(5):745–751

    Article  Google Scholar 

  13. Gomes AJ, Lunardi LO, Marchetti JM, Lunardi CN, Tedesco AC (2006) Indocyanine green nanoparticles useful for photomedicine. Photomed Laser Surg 24(4):514–521

    Article  CAS  Google Scholar 

  14. Raut CP, Sethi KS, Kohale BR, Mamajiwala A, Warang A (2018) Indocyanine green-mediated photothermal therapy in treatment of chronic periodontitis: a clinico-microbiological study. J Indian Soc Periodontol 22(3):221–227

    Article  Google Scholar 

  15. Shingnapurkar SH, Mitra DK, Kadav MS, Shah RA, Rodrigues SV, Prithyani SS (2016) The effect of indocyanine green-mediated photodynamic therapy as an adjunct to scaling and root planing in the treatment of chronic periodontitis: a comparative split-mouth randomized clinical trial. Indian J Dent Res 27(6):609–617

    Article  Google Scholar 

  16. Souza RC, Junqueira JC, Rossoni RD, Pereira CA, Munin E, Jorge AO (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(3):385–389

    Article  Google Scholar 

  17. Carmello JC, Alves F, Basso FG, de Souza Costa CA, Bagnato VS, de Oliveira Mima EG, Pavarina AC (2016) Treatment of oral candidiasis using photodithazine-mediated photodynamic therapy in vivo. PloS One 11 (6):e0156947

  18. Freire F, Ferraresi C, Jorge AOC, Hamblin MR (2016) Photodynamic therapy of oral Candida infection in a mouse model. J Photochem Photobiol B 159(1):161–168

    Article  CAS  Google Scholar 

  19. Azizi A, Amirzadeh Z, Rezai M, Lawaf S, Rahimi A (2016) Effect of photodynamic therapy with two photosensitizers on Candida albicans. J Photochem Photobiol B 158:267–273

    Article  CAS  Google Scholar 

  20. Pereira-Correia C, Costa A, Rasteiro V, Beltrame M, Junqueira JC, Jorge A (2011) Susceptibility of Candida albicans and Candida dubliniensis planktonic cultures and biofilms to erythrosine-and LED-mediated photodynamic therapy. Mycoses 56(11):1299–1305

    Google Scholar 

  21. Topaloglu N, Güney M, Yuksel S, Gülsoy M (2015) Antibacterial photodynamic therapy with 808-nm laser and indocyanine green on abrasion wound models. J Biomed Opt 20(2):280031–280037

    Article  Google Scholar 

  22. Seneviratne CJ, Silva WJ, Jin L, Samaranayake Y, Samaranayake L (2009) Architectural analysis, viability assessment and growth kinetics of Candida albicans and Candida glabrata biofilms. Arch Oral Biol 54(11):1052–1060

    Article  CAS  Google Scholar 

  23. Paz-Cristobal M, Royo D, Rezusta A, Andrés-Ciriano E, Alejandre M, Meis J, Revillo M, Aspiroz C, Nonell S, Gilaberte Y (2014) Photodynamic fungicidal efficacy of hypericin and dimethyl methylene blue against azole-resistant Candida albicans strains. Mycoses 57(1):35–42

    Article  CAS  Google Scholar 

  24. Saxena V, Sadoqi M, Shao J (2003) Degradation kinetics of indocyanine green in aqueous solution. J Pharm Sci 92(10):2090–2097

    Article  CAS  Google Scholar 

  25. Mindt S, Karampinis I, John M, Neumaier M, Nowak K (2018) Stability and degradation of indocyanine green in plasma, aqueous solution and whole blood. Photochem Photobiol Sci 17(9):1189–1196

    Article  CAS  Google Scholar 

  26. Pourhajibagher M, Kazemian H, Chiniforush N, Hosseini N, Pourakbari B, Azizollahi A, Rezaei F, Bahador A (2018) Exploring different photosensitizers to optimize elimination of planktonic and biofilm forms of Enterococcus faecalis from infected root canal during antimicrobial photodynamic therapy. Photochem Photobiol Sci 24:206–211

    CAS  Google Scholar 

  27. Beltes C, Economides N, Sakkas H, Papadopoulou C, Lambrianidis T (2017) Evaluation of antimicrobial photodynamic therapy using indocyanine green and near-infrared diode laser against Enterococcus faecalis in infected human root canals. Photomed Laser Surg 35(5):264–269

    Article  CAS  Google Scholar 

  28. Wong T-W, Liao S-Z, Ko W-C, Wu C-J, Wu SB, Chuang Y-C, Huang I (2019) Indocyanine green-mediated photodynamic therapy reduces methicillin-resistant Staphylococcus aureus drug resistance. J Clin Med 8(3):411–430

    Article  CAS  Google Scholar 

  29. Topaloglu N, Yuksel S, Gulsoy M (2013) Influence of different output powers on the efficacy of photodynamic therapy with 809-nm diode laser and indocyanine green. Proc SPIE 8579(85790H):1–6

    Google Scholar 

  30. Sasaki Y, Hayashi J-i, Fujimura T, Iwamura Y, Yamamoto G, Nishida E, Ohno T, Okada K, Yamamoto H, Kikuchi T (2017) New irradiation method with indocyanine green-loaded nanospheres for inactivating periodontal pathogens. Int J Mol Sci 18(1):154–164

    Article  Google Scholar 

  31. Dovigo LN, Pavarina AC, de Oliveira Mima EG, 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

    Article  CAS  Google Scholar 

  32. Basso FG, Oliveira CF, Fontana A, Kurachi C, Bagnato VS, Spolidório DM, Hebling J, Costa CA (2011) In vitro effect of low-level laser therapy on typical oral microbial biofilms. Braz Dent J 22(6):502–510

    Article  Google Scholar 

  33. Lambrechts S, Aalders M, Van Marle J (2005) Mechanistic study of the photodynamic inactivation of Candida albicans by a cationic porphyrin. Antimicrob Agents Chemother 49(5):2026–2034

    Article  CAS  Google Scholar 

  34. Bliss JM, Bigelow CE, Foster TH, Haidaris CG (2004) Susceptibility of Candida species to photodynamic effects of photofrin. Antimicrob Agents Chemother 48(6):2000–2006

    Article  CAS  Google Scholar 

  35. Chabrier-Roselló Y, Foster TH, Pérez-Nazario N, Mitra S, Haidaris CG (2005) Sensitivity of Candida albicans germ tubes and biofilms to photofrin-mediated phototoxicity. Antimicrob Agents Chemother 49(10):4288–4295

    Article  Google Scholar 

  36. Monfrecola G, Procaccini EM, Bevilacqua M, Manco A, Calabrò G, Santoianni P (2004) In vitro effect of 5-aminolaevulinic acid plus visible light on Candida albicans. Photochem Photobiol Sci 3(5):419–422

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Vice-Chancellor for Research Affairs of Shiraz University of Medical Sciences, Shiraz, Iran for their financial support (grant no. 16549). The authors wish to thank Dr. Laleh Khojasteh at the Research Consultation Center (RCC) of Shiraz University of Medical Sciences for her invaluable assistance in editing this manuscript. This manuscript is based on a thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Dental Medicine by Omid Kamrani.

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  1. Oral and Dental Disease Research Center, Department of Oral and Maxillofacial Medicine, School of Dentistry, Shiraz University of Medical Sciences, Shiraz, Iran

    Maryam Mardani & Omid Kamrani

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  1. Maryam Mardani
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Correspondence to Omid Kamrani.

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Mardani, M., Kamrani, O. Effectiveness of antimicrobial photodynamic therapy with indocyanine green against the standard and fluconazole-resistant Candida albicans. Lasers Med Sci 36, 1971–1977 (2021). https://doi.org/10.1007/s10103-021-03389-9

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