Antimicrobial photodynamic therapy: an effective alternative approach to control fungal infections

Skin mycoses are caused mainly by dermatophytes, which are fungal species that primarily infect areas rich in keratin such as hair, nails, and skin. Significantly, there are increasing rates of antimicrobial resistance among dermatophytes, especially for Trichophyton rubrum, the most frequent etiologic agent worldwide. Hence, investigators have been developing new therapeutic approaches, including photodynamic treatment. Photodynamic therapy (PDT) utilizes a photosensitive substance activated by a light source of a specific wavelength. The photoactivation induces cascades of photochemicals and photobiological events that cause irreversible changes in the exposed cells. Although photodynamic approaches are well established experimentally for the treatment of certain cutaneous infections, there is limited information about its mechanism of action for specific pathogens as well as the risks to healthy tissues. In this work, we have conducted a comprehensive review of the current knowledge of PDT as it specifically applies to fungal diseases. The data to date suggests that photodynamic treatment approaches hold great promise for combating certain fungal pathogens, particularly dermatophytes.

[1]  David W. Denning,et al.  Hidden Killers: Human Fungal Infections , 2012, Science Translational Medicine.

[2]  B. Kim,et al.  Photodynamic therapy: New treatment for recalcitrant Malassezia folliculitis , 2010, Lasers in surgery and medicine.

[3]  David Woolfson,et al.  Designing photosensitizers for photodynamic therapy: strategies, challenges and promising developments. , 2009, Future medicinal chemistry.

[4]  B. Elewski,et al.  Guidelines of care for superficial mycotic infections of the skin: onychomycosis. Guidelines/Outcomes Committee. American Academy of Dermatology. , 1996, Journal of the American Academy of Dermatology.

[5]  J. Lademann,et al.  Antifungal effect of 5‐aminolevulinic acid PDT in Trichophyton rubrum , 2005, Mycoses.

[6]  M. Calin,et al.  Light sources for photodynamic inactivation of bacteria , 2009, Lasers in Medical Science.

[7]  Michael R Hamblin,et al.  Concepts and Principles of Photodynamic Therapy as an Alternative Antifungal Discovery Platform , 2012, Front. Microbio..

[8]  Michael R Hamblin,et al.  Cutaneous sporotrichosis treated with photodynamic therapy: an in vitro and in vivo study. , 2014, Photomedicine and laser surgery.

[9]  D. A. Santos,et al.  Cryptococcus gattii: In Vitro Susceptibility to Photodynamic Inactivation , 2011, Photochemistry and photobiology.

[10]  Christina A. Cuomo,et al.  Fungi on the skin: dermatophytes and Malassezia. , 2014, Cold Spring Harbor perspectives in medicine.

[11]  A. Friedman,et al.  Trichophyton rubrum is Inhibited by Free and Nanoparticle Encapsulated Curcumin by Induction of Nitrosative Stress after Photodynamic Activation , 2015, PloS one.

[12]  P. Hynninen,et al.  Research advances in the use of tetrapyrrolic photosensitizers for photodynamic therapy. , 2004, Journal of photochemistry and photobiology. B, Biology.

[13]  T. Smijs,et al.  The Susceptibility of Dermatophytes to Photodynamic Treatment with Special Focus on Trichophyton rubrum , 2011, Photochemistry and photobiology.

[14]  Michael R Hamblin,et al.  Cell Death Pathways in Photodynamic Therapy of Cancer , 2011, Cancers.

[15]  J. C. Junqueira,et al.  Photodynamic therapy for the treatment of buccal candidiasis in rats , 2009, Lasers in Medical Science.

[16]  L. Cowen,et al.  The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype , 2008, Nature Reviews Microbiology.

[17]  David S. Jones,et al.  Photosensitisers – the progression from photodynamic therapy to anti-infective surfaces , 2015, Expert opinion on drug delivery.

[18]  B. Piraccini,et al.  Photodynamic therapy of onychomycosis caused by Trichophyton rubrum. , 2008, Journal of the American Academy of Dermatology.

[19]  Cristina Kurachi,et al.  Investigation of the Photodynamic Effects of Curcumin Against Candida albicans , 2011, Photochemistry and photobiology.

[20]  Q. Peng,et al.  Apoptosis and necrosis induced with light and 5-aminolaevulinic acid-derived protoporphyrin IX. , 1996, British Journal of Cancer.

[21]  M. Ghannoum,et al.  Clinical Trichophyton rubrum Strain Exhibiting Primary Resistance to Terbinafine , 2003, Antimicrobial Agents and Chemotherapy.

[22]  V. Bagnato,et al.  Curcumin-mediated photodynamic inactivation of Candida albicans in a murine model of oral candidiasis. , 2013, Medical mycology.

[23]  M. Costa,et al.  The photodynamic effect of methylene blue and toluidine blue on Candida albicans is dependent on medium conditions , 2009, The Journal of Microbiology.

[24]  A. S. Queiroga,et al.  In vitro photodynamic inactivation of Candida spp. by different doses of low power laser light. , 2011, Photodiagnosis and photodynamic therapy.

[25]  E. Munin,et al.  Study of germ tube formation by Candida albicans after photodynamic antimicrobial chemotherapy (PACT). , 2007, Journal of photochemistry and photobiology. B, Biology.

[26]  Lívia Nordi Dovigo,et al.  Susceptibility of Candida albicans to photodynamic therapy in a murine model of oral candidosis. , 2010, Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics.

[27]  Z. Fedorowicz,et al.  Topical antifungal treatments for tinea cruris and tinea corporis. , 2014, The Cochrane database of systematic reviews.

[28]  T. Foster,et al.  Effective photosensitization and selectivity In Vivo of Candida Albicans by meso‐tetra (N‐methyl‐4‐pyridyl) porphine tetra tosylate , 2011, Lasers in surgery and medicine.

[29]  J. Usuda,et al.  Photodynamic therapy (PDT) for lung cancers. , 2006, Journal of thoracic oncology : official publication of the International Association for the Study of Lung Cancer.

[30]  D. A. Santos,et al.  Photodynamic therapy efficiently controls dermatophytosis caused by Trichophyton rubrum in a murine model , 2015, British Journal of Dermatology.

[31]  T. Smijs,et al.  Photodynamic Inactivation of the Dermatophyte Trichophyton rubrum¶ , 2003, Photochemistry and photobiology.

[32]  Michael R Hamblin,et al.  Effect of charge on the interaction of site-specific photoimmunoconjugates with human ovarian cancer cells. , 1996, Cancer research.

[33]  A. Tedesco,et al.  In Vitro Photodynamic Inactivation of Cryptococcus neoformans Melanized Cells with Chloroaluminum Phthalocyanine Nanoemulsion , 2012, Photochemistry and photobiology.

[34]  F. Harris,et al.  Photodynamic therapy based on 5‐aminolevulinic acid and its use as an antimicrobial Agent , 2012, Medicinal research reviews.

[35]  E J BALDES,et al.  The photodynamic properties of a particular hematoporphyrin derivative. , 1960, Archives of dermatology.

[36]  B. Elewski,et al.  Guidelines of care for superficial mycotic infections of the skin: tinea capitis and tinea barbae. Guidelines/Outcomes Committee. American Academy of Dermatology. , 1996, Journal of the American Academy of Dermatology.

[37]  Jos. Seherer Chemisch‐physiologische Untersuchungen , 1841 .

[38]  M. Hahne,et al.  Cell Death , 2010, Cell Death and Differentiation.

[39]  P. Calzavara-Pinton,et al.  A comprehensive overview of photodynamic therapy in the treatment of superficial fungal infections of the skin. , 2005, Journal of photochemistry and photobiology. B, Biology.

[40]  Aditya K. Gupta,et al.  Laser Therapy for Onychomycosis , 2013, Journal of cutaneous medicine and surgery.

[41]  H. van den Bergh,et al.  Like a Bolt from the Blue: Phthalocyanines in Biomedical Optics , 2011, Molecules.

[42]  J E Kaufman,et al.  Photoradiation therapy for the treatment of malignant tumors. , 1978, Cancer research.

[43]  A. Espinel-Ingroff,et al.  Treatment of refractory fingernail onychomycosis caused by nondermatophyte molds with methylaminolevulinate photodynamic therapy. , 2011, Journal of the American Academy of Dermatology.

[44]  Michael R Hamblin,et al.  Photodynamic therapy: a new antimicrobial approach to infectious disease? , 2004, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[45]  P. Cisalpino,et al.  In vitro photodynamic inactivation of Candida spp. growth and adhesion to buccal epithelial cells. , 2009, Journal of photochemistry and photobiology. B, Biology.

[46]  Rosa Maria Machado-de-sena,et al.  Photodynamic therapy has antifungal effect and reduces inflammatory signals in Candida albicans-induced murine vaginitis. , 2014, Photodiagnosis and photodynamic therapy.

[47]  Michael R Hamblin,et al.  Blue Dye and Red Light, a Dynamic Combination for Prophylaxis and Treatment of Cutaneous Candida albicans Infections in Mice , 2011, Antimicrobial Agents and Chemotherapy.

[48]  T. Fitzpatrick,et al.  The evolution of photochemotherapy with psoralens and UVA (PUVA): 2000 BC to 1992 AD. , 1992, Journal of photochemistry and photobiology. B, Biology.

[49]  D. A. Santos,et al.  Photodynamic inhibition of Trichophyton rubrum: in vitro activity and the role of oxidative and nitrosative bursts in fungal death. , 2013, The Journal of antimicrobial chemotherapy.

[50]  E. Munin,et al.  Photodynamic antimicrobial chemotherapy (PACT) with methylene blue increases membrane permeability in Candida albicans , 2007, Lasers in Medical Science.

[51]  C. J. de Lima,et al.  In vitro photodynamic therapy against Foncecaea pedrosoi and Cladophialophora carrionii , 2013, Mycoses.

[52]  You Chan Kim,et al.  Successful treatment of pityriasis versicolor with 5-aminolevulinic acid photodynamic therapy. , 2007, Archives of dermatology.

[53]  V. Bagnato,et al.  Comparison of Photodynamic Therapy versus conventional antifungal therapy for the treatment of denture stomatitis: a randomized clinical trial. , 2012, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[54]  B. Elewski,et al.  Guidelines of care for superficial mycotic infectionsof the skin: Tinea capitis and tinea barbae , 1996 .

[55]  Seamus J. Martin,et al.  Dose‐dependent induction of apoptosis in human tumour cell lines by widely diverging stimuli , 1991, Cell proliferation.

[56]  Michael R Hamblin,et al.  Selective photoinactivation of Candida albicans in the non-vertebrate host infection model Galleria mellonella , 2013, BMC Microbiology.

[57]  M. Venturini,et al.  Photodynamic Antifungal Chemotherapy † , 2012, Photochemistry and photobiology.

[58]  R. Summerbell,et al.  The dermatophytes , 1995, Clinical microbiology reviews.

[59]  Michael R Hamblin,et al.  Susceptibility of Cryptococcus neoformans to Photodynamic Inactivation Is Associated with Cell Wall Integrity , 2007, Antimicrobial Agents and Chemotherapy.

[60]  S. Grunewald,et al.  Laser therapy of onychomycosis , 2014, Journal der Deutschen Dermatologischen Gesellschaft = Journal of the German Society of Dermatology : JDDG.

[61]  F. Berr,et al.  Photophysics and photochemistry of photodynamic therapy: fundamental aspects , 2009, Lasers in Medical Science.

[62]  M. Hamblin,et al.  Photodynamic Therapy Combined with Terbinafine Against Chromoblastomycosis and the Effect of PDT on Fonsecaea monophora In Vitro , 2014, Mycopathologia.

[63]  A. Napier Skin Diseases , 1889, Health technology directions.

[64]  Aditya K. Gupta,et al.  Update in Antifungal Therapy of Dermatophytosis , 2008, Mycopathologia.

[65]  P. Nenoff,et al.  Mycology – an update. Part 1: Dermatomycoses: Causative agents, epidemiology and pathogenesis , 2014, Journal der Deutschen Dermatologischen Gesellschaft = Journal of the German Society of Dermatology : JDDG.

[66]  Vanya Mantareva,et al.  Photodynamic efficacy of water-soluble Si(IV) and Ge(IV) phthalocyanines towards Candida albicans planktonic and biofilm cultures. , 2011, European journal of medicinal chemistry.

[67]  M. Biel,et al.  Treatment of oral candidiasis with methylene blue-mediated photodynamic therapy in an immunodeficient murine model. , 2002, Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics.

[68]  Z. Apalla,et al.  Photodynamic therapy for distal and lateral subungual toenail onychomycosis caused by Trichophyton rubrum: Preliminary results of a single-centre open trial. , 2010, Acta dermato-venereologica.

[69]  P. McCarron,et al.  Antifungal photodynamic therapy. , 2008, Microbiological research.

[70]  A. Bruni,et al.  The photodynamic effect of 5-(4-hydroxy-1-butinyl)-2,2′-bithienyl on dermatophytes , 1998 .

[71]  E. Durantini,et al.  Photodynamic inactivation of Candida albicans sensitized by tri- and tetra-cationic porphyrin derivatives. , 2009, European journal of medicinal chemistry.

[72]  Hidetoshi Takahashi,et al.  Antifungal effect of TONS504‐photodynamic therapy on Malassezia furfur , 2014, The Journal of dermatology.

[73]  M. J. Mendes-Giannini,et al.  Highlights in pathogenic fungal biofilms. , 2014, Revista iberoamericana de micologia.

[74]  A. Velegraki,et al.  Skin diseases associated with Malassezia yeasts: facts and controversies. , 2013, Clinics in dermatology.

[75]  R. Prasad,et al.  Antifungal curcumin induces reactive oxygen species and triggers an early apoptosis but prevents hyphae development by targeting the global repressor TUP1 in Candida albicans. , 2010, Bioscience reports.

[76]  C. Enderlin Chemisch‐physiologische Untersuchungen , 1848 .

[77]  Michael R Hamblin,et al.  Influence of multidrug efflux systems on methylene blue-mediated photodynamic inactivation of Candida albicans. , 2011, The Journal of antimicrobial chemotherapy.

[78]  M. A. Resende,et al.  Photodynamic Antifungal Therapy Against Chromoblastomycosis , 2011, Mycopathologia.

[79]  Michael R Hamblin,et al.  Effect of Virulence Factors on the Photodynamic Inactivation of Cryptococcus neoformans , 2013, PloS one.