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Effects of Photodynamic Therapy on the Growth and Antifungal Susceptibility of Scedosporium and Lomentospora spp.

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Abstract

Scedosporium and Lomentospora species are the second most frequent colonizing, allergenic, or invasive fungal pathogens in patients with cystic fibrosis, and are responsible for infections varying from cutaneous and subcutaneous tissue infections caused by traumatic inoculation to severe systemic diseases in immunocompromised patients. The clinical relevance of fungal airway colonization for individual patients harboring Scedosporium and Lomentospora species is still an underestimated issue. The high resistance of Scedosporium and Lomentospora species to antifungal drugs has highlighted the need for alternative treatment modalities, and antimicrobial photodynamic therapy may be one such alternative. In this study, methylene blue was applied as a photosensitizing agent to 6 type strains of Scedosporium and Lomentospora species, and we irradiated the strains using a light-emitting diode (635 ± 10 nm, 12 J/cm2). We evaluated the effects of photodynamic therapy on strain growth and on the in vitro susceptibility of the strains to itraconazole, voriconazole, posaconazole, and amphotericin B. A colony-forming unit reduction of up to 5.2 log10 was achieved. Minimal inhibitory concentration ranges also decreased significantly with photoinactivation. Photodynamic therapy improved both the inactivation rates and the antifungal susceptibility profile of all fungal isolates tested.

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References

  1. Cortez KJ, Roilides E, Quiroz-Telles F, Meletiadis J, Antachopoulos C, Knudsen T, Buchanan W, Milanovich J, Sutton DA, Fothergill A, Rinaldi MG, Shea YR, Zaoutis T, Kottilil S, Walsh TJ. Infections caused by Scedosporium spp. Clin Microbiol Rev. 2008;21:157–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Kaltseis J, Rainer J, de Hoog GS. Ecology of Pseudallescheria and Scedosporium species in human-dominated and natural environments and their distribution in clinical samples. Med Mycol. 2009;47:398–405.

    Article  CAS  PubMed  Google Scholar 

  3. Lackner M, Guarro J. Pathogenesis of Scedosporium. Curr Fungal Infect Rep. 2013;7:326–33.

    Article  Google Scholar 

  4. Guignard S, Hubert D, Dupont B, Anract P, Alioua D, Guerini H, Paugam A, Dougados M. Multifocal Scedosporium apiospermum spondylitis in a cystic fibrosis patient. J Cyst Fibros. 2008;7:89–91.

    Article  CAS  PubMed  Google Scholar 

  5. Koch C, Høiby N. Diagnosis and treatment of cystic fibrosis. Respiration. 2000;67:239–47.

    Article  CAS  PubMed  Google Scholar 

  6. Lam SM, Lau AC, Ma MW, Yam LY. Pseudallescheria boydii or Aspergillus fumigatus in a lady with an unresolving lung infiltrate, and a literature review. Respirology. 2008;13:478–80.

    Article  PubMed  Google Scholar 

  7. Gilgado F, Serena C, Cano J, Gené J, Guarro J. Antifungal susceptibilities of the species of the Pseudallescheria boydii complex. Antimicrob Agents Chemother. 2006;50:4211–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Pihet M, Carrere J, Cimon B, Chabasse D, Delhaes L, Symoens F, Bouchara JP. Occurrence and relevance of filamentous fungi in respiratory secretions of patients with cystic fibrosis—a review. Med Mycol. 2009;47:387–97.

    Article  PubMed  Google Scholar 

  9. Sedlacek L, Graf B, Schwarz C, Albert F, Peter S, Wurstl B, Wagner S, Klotz M, Becker A, Haase G, Laniado G, Kahl B, Suerbaum S, Seibold M, Tintelnot K. Prevalence of Scedosporium species and Lomentospora prolificans in patients with cystic fibrosis in a multicenter trial by use of a selective medium. J Cyst Fibros. 2015;14:237–41.

    Article  CAS  PubMed  Google Scholar 

  10. Lackner M, de Hoog GS, Verweij PE, Najafzadeh MJ, Curfs-Breuker I, Klaassen CH, Meis JF. Species-specific antifungal susceptibility patterns of Scedosporium and Pseudallescheria species. Antimicrob Agents Chemother. 2012;56:2635–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. St Denis TG, Dai T, Izikson L, Astrakas C, Anderson RR, Hamblin MR, Tegos GP. All you need is light: antimicrobial photoinactivation as an evolving and emerging discovery strategy against infectious disease. Virulence. 2011;2:509–20.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Calin MA, Parasca SV. Light sources for photodynamic inactivation of bacteria. Lasers Med Sci. 2009;24:453–60.

    Article  PubMed  Google Scholar 

  13. Moreira LM, Santos FV, Lyon JP, Maftoum-Costa M, Pacheco-Soares C, Silva NS. Photodynamic therapy: porphyrins and phthalocyanines as photosensitizers. Aust J Chem. 2008;61:741–54.

    Article  CAS  Google Scholar 

  14. Hamblin MR, Hasan T. Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem Photobiol Sci. 2004;3:436–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wainwright M, Maisch T, Nonell S, Plaetzer K, Almeida A, Tegos GP, Hamblin MR. Photoantimicrobials-are we afraid of the light? Lancet Infect Dis. 2017;17:e49–55.

    Article  PubMed  Google Scholar 

  16. Lyon JP, Moreira LM, de Carvalho VS, dos Santos FV, de Lima CJ, de Resende MA. In vitro photodynamic therapy against Foncecaea pedrosoi and Cladophialophora carrionii. Mycoses. 2013;56:157–61.

    Article  PubMed  Google Scholar 

  17. Nunes Mario DA, Denardi LB, Brayer Pereira DI, Santurio JM, Alves SH. In vitro photodynamic inactivation of Sporothrix schenckii complex species. Med Mycol. 2014;52:770–3.

    Article  PubMed  Google Scholar 

  18. Gao L, Jiang S, Sun Y, Deng M, Wu Q, Li M, Zeng T. Evaluation of the effects of photodynamic therapy alone and combined with standard antifungal therapy on planktonic cells and biofilms of Fusarium spp. and Exophiala spp. Front Microbiol. 2016;7:617.

    PubMed  PubMed Central  Google Scholar 

  19. Lyon JP, Pedroso e Silva Azevedo Cde M, Moreira LM, de Lima CJ, de Resende MA. Photodynamic antifungal therapy against chromoblastomycosis. Mycopathologia. 2011;172:293–7.

    Article  CAS  PubMed  Google Scholar 

  20. Dai T, Bil de Arce VJ, Tegos GP, Hamblin MR. Blue dye and red light, a dynamic combination for prophylaxis and treatment of cutaneous Candida albicans infections in mice. Antimicrob Agents Chemother. 2011;55:5710–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Souza LW, Souza SV, Botelho AC. Distal and lateral toenail onychomycosis caused by Trichophyton rubrum: treatment with photodynamic therapy based on methylene blue dye. An Bras Dermatol. 2014;89:184–6.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Gilaberte Y, Aspiroz C, Martes MP, Alcalde V, Espinel-Ingroff A, Rezusta A. Treatment of refractory fingernail onychomycosis caused by nondermatophyte molds with methylaminolevulinate photodynamic therapy. J Am Acad Dermatol. 2011;65:669–71.

    Article  PubMed  Google Scholar 

  23. Qiao J, Li R, Ding Y, Fang H. Photodynamic therapy in the treatment of superficial mycoses: an evidence-based evaluation. Mycopathologia. 2010;170:339–43.

    Article  PubMed  Google Scholar 

  24. Sotiriou E, Koussidou-Eremonti T, Chaidemenos G, Apalla Z, Ioannides D. Photodynamic therapy for distal and lateral subungual toenail onychomycosis caused by Trichophyton rubrum: preliminary results of a single-centre open trial. Acta Derm Venereol. 2010;90:216–7.

    Article  PubMed  Google Scholar 

  25. Dos Santos LF, Melo NB, de Carli ML, Mendes AC, Bani GM, Verinaud LM, Burger E, de Oliveira I, Moraes G, Pereira AA, Brigagão MR, Hanemann JA, Sperandio FF. Photodynamic inactivation of Paracoccidioides brasiliensis helps the outcome of oral paracoccidiodomycosis. Lasers Med Sci. 2017;. doi:10.1007/s10103-017-2193-y-&gt.

    Google Scholar 

  26. Institute CaLS. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi. Approved Standard. M38-A2; 2008.

  27. Tintelnot K, Just-Nubling G, Horre R, Graf B, Sobottka I, Seibold M, Haas A, Kaben U, De Hoog GS. A review of German Scedosporium prolificans cases from 1993 to 2007. Med Mycol. 2009;47:351–8.

    Article  CAS  PubMed  Google Scholar 

  28. Mima EG, Pavarina AC, Dovigo LN, Vergani CE, Costa CAdS, Kurachi C, Bagnato VS. Susceptibility of Candida albicans to photodynamic therapy in a murine model of oral candidosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;109:392–401.

    Article  PubMed  Google Scholar 

  29. Černáková L, Dižová S, Bujdáková H. Employment of methylene blue irradiated with laser light source in photodynamic inactivation of biofilm formed by Candida albicans strain resistant to fluconazole. Med Mycol. 2017. doi:10.1093/mmy/myw137.

    PubMed  Google Scholar 

  30. Giroldo LM, Felipe MP, de Oliveira MA, Munin E, Alves LP, Costa MS. Photodynamic antimicrobial chemotherapy (PACT) with methylene blue increases membrane permeability in Candida albicans. Lasers Med Sci. 2009;24:109–12.

    Article  PubMed  Google Scholar 

  31. Lyon JP, Carvalho CR, Rezende RR, Lima CJ, Santos FV, Moreira LM. Synergism between fluconazole and methylene blue-photodynamic therapy against fluconazole-resistant Candida strains. Indian J Med Microbiol. 2016;34:506–8.

    Article  CAS  PubMed  Google Scholar 

  32. Jori G. Photodynamic therapy of microbial infections: state of the art and perspectives. J Environ Pathol Toxicol Oncol. 2006;25:505–19.

    Article  PubMed  Google Scholar 

  33. Cai X, Li W, Zhang L, Wang X, Luo R, Li L. Photodynamic therapy for intractable bronchial lung cancer. Photodiagn Photodyn Ther. 2013;10:672–6.

    Article  Google Scholar 

  34. Luigi Corti, Lamberto Toniolo, Caterina Boso, Flavio Colaut, Davide Fiore, Pier-Carlo Muzzio, Lucio Loreggian, Guido Sotti. Endoscopic treatment of early bronchial cancer: our experience with photodynamic therapy (PDT). Proc SPIE. 2009;7380:1–11.

    Google Scholar 

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Acknowledgements

We gratefully acknowledge Professor Sybren de Hoog from the Centraalbureau voor Schimmelcultures Fungal Biodiversity Centre (CBS), Utrecht, The Netherlands, for kindly providing us with the strains studied. In addition, we thank Professor Elena Piecková from Slovak Medical University, Slovakia, for excellent guidance with regard to the data analysis.

Funding

This work was supported by the National Natural Science Foundation of China (81401713 to Qiaoyun Lu, 31400131 to Lujuan Gao, and 81401677 to Yi Sun), the Outstanding Youth Project of Zhongshan Hospital, Fudan University (2015ZSYXQN21 to Lujuan Gao), and the Hubei Provincial Health and Family Planning Scientific Research Project (WJ2015MB281 to Yi Sun).

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Correspondence to Qiaoyun Lu or Lujuan Gao.

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Lu, Q., Sun, Y., Tian, D. et al. Effects of Photodynamic Therapy on the Growth and Antifungal Susceptibility of Scedosporium and Lomentospora spp.. Mycopathologia 182, 1037–1043 (2017). https://doi.org/10.1007/s11046-017-0195-8

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  • DOI: https://doi.org/10.1007/s11046-017-0195-8

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