El Impacto del azul de metileno en la terapia fotodinámica antimicrobiana contra diferentes especies de Candida y la sinergia con fluconazol
D.I. Loaiza-Toscuento, D. Vazquez-Dominguez, A.P. Texis-Espinosa, J.C. Ramírez-San-Juan, R. Ramos-García, T. Spezzia-Mazzocco
Descargar artículo
Información básica
Volumen
V57 - N1 / 2024 Especial: RIAO OPTILAS 2023
Referencia
51159
DOI
http://dx.doi.org/10.7149/OPA.57.1.51159
Idioma
English
Etiquetas
Azul de metileno, resistencia antifúngica, Candida sp., terapia fotodinámica antimicrobiana, fluconazol, tratamiento sinérgico
Resumen
La resistencia antifúngica en las cepas de Candida ha aumentado recientemente, especialmente en las cepas de Candida no-albicans, lo que hace que el desarrollo de tratamientos alternativos para las infecciones fúngicas sea crítico. La terapia fotodinámica antimicrobiana (TFDa) es un tratamiento alternativo prometedor que se ha utilizado con éxito contra diversas infecciones y microorganismos, incluida Candida albicans. Sin embargo, todavía son limitados los estudios sobre cepas de C. non-albicans, como Candida tropicalis y Candida glabrata. En este trabajo se evaluó el efecto de la aPDT en 18 cepas de 3 especies de Candida: (C. albicans, C. tropicalis y C. glabrata). Además, se realizaron tratamientos sinérgicos con fluconazol y aPDT empleando azul de metileno (MB) como fotosensibilizador (FS) en una cepa de C. albicans y una de C. tropicalis. La resistencia a los azoles se evaluó mediante el método de difusión en disco de Kirby y Bauer y la captación de MB intracelular mediante lisis celular y análisis espectroscópico. Nuestros resultados mostraron que la aPDT usando MB como FS inhibía efectivamente el crecimiento de todas las cepas de levadura probadas in vitro. Incluso cepas resistentes a fluconazol, menos estudiadas, como C. glabrata o C. tropicalis mostraron una inhibición significativa, independientemente de las diferencias en la resistencia a los fármacos, el origen de aislamiento de las cepas o la concentración intracelular de MB. También se observaron efectos sinérgicos de la TFDA con fluconazol, dosis subletales de aPDT más fluconazol eliminaron las cepas resistentes (C. tropicalis) o sensibles (C. albicans) a fluconazol. Lo que sugiere que la aPDT es un tratamiento alternativo viable para muchas especies de Candida, solo o en combinación con medicamentos antimicóticos.
Referencias
N. Martins, I. C. F. R. Ferreira, L. Barros, S. Silva, and M. Henriques, “Candidiasis: Predisposing Factors, Prevention, Diagnosis and Alternative Treatment,” Mycopathologia 177, 223–240 (2014).
M. A. Pfaller and D. J. Diekema, “Epidemiology of Invasive Candidiasis: a Persistent Public Health Problem,” Clin. Microbiol. Rev., 20, 133–163 (2007).
R. Sandhu, S. Dahiya, P. Sayal, and D. Budhani, “Increased role of nonalbicans Candida, potential risk factors, and attributable mortality in hospitalized patients,” J. Heal. Res. Rev. 4, 78 (2017).
M. Taha and A. B. Zaghloul, “Superficial Fungal Infections,” in Pigmented Ethnic Skin and Imported Dermatoses, Cham: Springer International Publishing, 37–51 (2018).
G. Quindós, C. Marcos-Arias, R. San-Millán, E. Mateo, and E. Eraso, “The continuous changes in the aetiology and epidemiology of invasive candidiasis: from familiar Candida albicans to multiresistant Candida auris,” Int. Microbiol., 21, 107–119 (2018).
S. A. Turner and G. Butler, “The Candida Pathogenic Species Complex,” Cold Spring Harb. Perspect. Med. 4, a019778–a019778 (2014).
G. Sadeghi, M. Ebrahimi-Rad, S. F. Mousavi, M. Shams-Ghahfarokhi, and M. Razzaghi-Abyaneh, “Emergence of non-Candida albicans species: Epidemiology, phylogeny and fluconazole susceptibility profile,” J. Mycol. Med. 28, 51–58 (2018).
T. P. McCarty et al., “Echinocandin resistance among Candida isolates at an academic medical centre 2005–15: analysis of trends and outcomes,” J. Antimicrob. Chemother. 73, 1677–1680 (2018).
M. Nucci, G. Barreiros, L. F. Guimarães, V. A. S. Deriquehem, A. C. Castiñeiras, and S. A. Nouér, “Increased incidence of candidemia in a tertiary care hospital with the COVID-19 pandemic,” Mycoses 64, 152–156 (2021).
C. V. W. Riche, R. Cassol, and A. C. Pasqualotto, “Is the Frequency of Candidemia Increasing in COVID-19 Patients Receiving Corticosteroids?,” J. Fungi 6, 286 (2020).
A. D. Alves, N. Gurgel-Juarez, A. C. Vieira, A. A. Proietti, and A. R. Pinheiro Barcessat, “PDT technology: an alternative to control oral candidiasis in critically ill patients,” Lasers Dent. Sci., 5, 193–197(2021).
M. C. Arendrup and T. F. Patterson, “Multidrug-Resistant Candida: Epidemiology, Molecular Mechanisms, and Treatment,” J. Infect. Dis. 216, S445–S451 (2017).
Y. Chong et al., “Fatal candidemia caused by azole-resistant Candida tropicalis in patients with hematological malignancies,” J. Infect. Chemother. 18, 41–746 (2012).
B. Timmermans, A. De Las Peñas, I. Castaño, and P. Van Dijck, “Adhesins in Candida glabrata,” J. Fungi 4, 60 (2018).
P. L. Fidel, J. A. Vazquez, and J. D. Sobel, “Candida glabrata : Review of Epidemiology, Pathogenesis, and Clinical Disease with Comparison to C. albicans,” Clin. Microbiol. Rev. 12, 80–96, (1999).
L. Benov, “Photodynamic Therapy: Current Status and Future Directions,” Med. Princ. Pract. 24,14– 28 (2015).
B. Krammer and T. Verwanger, “Molecular Biological Mechanisms in Photodynamic Therapy,” in Photodynamic Therapy, Berlin, Heidelberg: Springer Berlin Heidelberg (2014).
M. H. Abdel-Kader, “History of Photodynamic Therapy,” in Photodynamic Therapy, Berlin, Heidelberg: Springer Berlin Heidelberg (2014).
F. Cieplik, L. Tabenski, W. Buchalla, and T. Maisch, “Antimicrobial photodynamic therapy for inactivation of biofilms formed by oral key pathogens,” Front. Microbiol. 5 (2014).
P. C. V. Conrado et al., “A systematic review of photodynamic therapy as an antiviral treatment: Potential guidance for dealing with SARS-CoV-2,” Photodiagnosis Photodyn. Ther. 34, 102221 (2021).
F. Cieplik et al., “Antimicrobial photodynamic therapy – what we know and what we don’t,” Crit. Rev. Microbiol. 44, 571–589 (2018).
L. M. Baltazar, A. Ray, D. A. Santos, P. S. Cisalpino, A. J. Friedman, and J. D. Nosanchuk, “Antimicrobial photodynamic therapy: an effective alternative approach to control fungal infections,” Front. Microbiol. 6 (2015).
L. Černáková, S. Dižová, and H. Bujdáková, “Employment of methylene blue irradiated with laser light source in photodynamic inactivation of biofilm formed by Candida albicans strain resistant to fluconazole,” Med. Mycol., p. myw137 (2017).
T. Q. Corrêa et al., “Photodynamic inactivation for in vitro decontamination of Staphylococcus aureus in whole blood,” Photodiagnosis Photodyn. Ther. 28, 58–64 (2019).
V. Sousa, A. T. P. C. Gomes, A. Freitas, M. A. F. Faustino, M. G. P. M. S. Neves, and A. Almeida, “Photodynamic Inactivation of Candida albicans in Blood Plasma and Whole Blood,” Antibiotics, 8, 221 (2019).
M. Bartolomeu, S. Reis, M. Fontes, M. Neves, M. Faustino, and A. Almeida, “Photodynamic Action against Wastewater Microorganisms and Chemical Pollutants: An Effective Approach with Low Environmental Impact,” Water 9, 630, Aug. (2017).
B. A. Garcia, B. H. D. Panariello, K. M. de Freitas Pontes, and S. Duarte, “Regimen and different surfaces interfere with photodynamic therapy on Candida albicans biofilms,” J. Microbiol. Methods, vol. 178, p. 106080, Nov. (2020).
X. Hu, Y.-Y. Huang, Y. Wang, X. Wang, and M. R. Hamblin, “Antimicrobial Photodynamic Therapy to Control Clinically Relevant Biofilm Infections,” Front. Microbiol., vol. 9, Jun. (2018).
S. A. Torres-Hurtado et al., “Efficient in vitro photodynamic inactivation using repetitive light energy density on Candida albicans and Trichophyton mentagrophytes,” Photodiagnosis Photodyn. Ther. 26, (2019).
A. Arastehfar et al., “Antifungal susceptibility, genotyping, resistance mechanism, and clinical profile of Candida tropicalis blood isolates,” Med. Mycol. 58, 766–773 (2020).
C. Jiang, Z. Li, L. Zhang, Y. Tian, D. Dong, and Y. Peng, “Significance of hyphae formation in virulence of Candida tropicalis and transcriptomic analysis of hyphal cells,” Microbiol. Res. 192, 65–72 (2016).
S. J. N. Duxbury, S. Bates, R. E. Beardmore, and I. Gudelj, “Evolution of drug-resistant and virulent small colonies in phenotypically diverse populations of the human fungal pathogen Candida glabrata,” Proc. R. Soc. B Biol. Sci. 287, 20200761 (2020).
A. Warris and E. R. Ballou, “Oxidative responses and fungal infection biology,” Semin. Cell Dev. Biol., 89, 34–46 (2019).
L. N. Dovigo, A. C. Pavarina, D. G. Ribeiro, C. S. Adriano, and V. S. Bagnato, “Photodynamic inactivation of four Candida species induced by photogem®,” Brazilian J. Microbiol. 41, 42–49, (2010).
M. J. Navarro-Arias et al., “Differential recognition of Candida tropicalis, Candida guilliermondii, Candida krusei, and Candida auris by human innate immune cells,” Infect. Drug Resist. 12, 783–794 (2019).
X. Guo et al., “Understand the genomic diversity and evolution of fungal pathogen Candida glabrata by genome-wide analysis of genetic variations,” Methods 176, 82–90, (2020).
L. Carreté et al., “Patterns of Genomic Variation in the Opportunistic Pathogen Candida glabrata Suggest the Existence of Mating and a Secondary Association with Humans,” Curr. Biol. 28, 15-27.e7 (2018).
L. de Carvalho Leonel, M. L. Carvalho, B. M. da Silva, S. Zamuner, C. Alberto-Silva, and M. Silva Costa, “Photodynamic Antimicrobial Chemotherapy (PACT) using methylene blue inhibits the viability of the biofilm produced by Candida albicans,” Photodiagnosis Photodyn. Ther., 26, 316–323 (2019).
Ö. Güzel Tunccan et al., “The in vitro effect of antimicrobial photodynamic therapy on Candida and Staphylococcus biofilms,” TURKISH J. Med. Sci. 48, 873–879 (2018).
N. Hosseini, S. Yazdanpanah, M. Saki, F. Rezazadeh, J. Ghapanchi, and K. Zomorodian, “Susceptibility of Candida albicans and Candida dubliniensis to Photodynamic Therapy Using Four Dyes as the Photosensitizer.,” J. Dent. (Shiraz, Iran), 17, 354–360 (2016).
M. A. Sherwani, S. Tufail, A. A. Khan, and M. Owais, “Gold Nanoparticle-Photosensitizer Conjugate Based Photodynamic Inactivation of Biofilm Producing Cells: Potential for Treatment of C. albicans Infection in BALB/c Mice,” PLoS One 10, p. e0131684 (2015).
R. D. Rossoni, J. O. Barbosa, F. E. de Oliveira, L. D. de Oliveira, A. O. C. Jorge, and J. C. Junqueira, “Biofilms of Candida albicans serotypes A and B differ in their sensitivity to photodynamic therapy,” Lasers Med. Sci. 29, 1679–1684 (2014).
A. S. Sousa et al., “Photodynamic inactivation of Candida albicans biofilm: Influence of the radiant energy and photosensitizer charge,” Photodiagnosis Photodyn. Ther. 14, 111–114 (2016).
L. S. de Figueiredo Freitas, R. D. Rossoni, A. O. C. Jorge, and J. C. Junqueira, “Repeated applications of photodynamic therapy on Candida glabrata biofilms formed in acrylic resin polymerized,” Lasers Med. Sci. 32, 549–555 (2017).
J. P. Lyon, R. R. Rezende, M. P. Rabelo, C. J. de Lima, and L. M. Moreira, “Synergic Effect of Photodynamic Therapy with Methylene Blue and Surfactants in the Inhibition of Candida albicans,” Mycopathologia 175, 159–164 (2013).
R. A. Prates, I. T. Kato, M. S. Ribeiro, G. P. Tegos, and M. R. Hamblin, “Influence of multidrug efflux systems on methylene blue-mediated photodynamic inactivation of Candida albicans,” J. Antimicrob. Chemother. 66, 1525–1532 (2011).
A. S. Queiroga, V. N. Trajano, E. O. Lima, A. F. M. Ferreira, A. S. Queiroga, and F. A. Limeira, “In vitro photodynamic inactivation of Candida spp. by different doses of low power laser light,” Photodiagnosis Photodyn. Ther. 8, 332–336 (2011).
J. P. Lyon, C. R. Carvalho, R. R. Rezende, C. J. Lima, F. V Santos, and L. M. Moreira, “Synergism between fluconazole and methylene blue - photodynamic therapy against fluconazole - resistant Candida strains,” Indian J. Med. Microbiol. 34, 506–508 (2016).
G. G. Carvalho, M. P. Felipe, and M. S. Costa, “The photodynamic effect of methylene blue and toluidine blue on Candida albicans is dependent on medium conditions,” J. Microbiol. 47, 619–623, (2009).
G. A. da Collina et al., “Controlling methylene blue aggregation: a more efficient alternative to treat Candida albicans infections using photodynamic therapy,” Photochem. Photobiol. Sci., 17, 1355– 1364 (2018).
F. Daliri, A. Azizi, M. Goudarzi, S. Lawaf, and A. Rahimi, “In vitro comparison of the effect of photodynamic therapy with curcumin and methylene blue on Candida albicans colonies,” Photodiagnosis Photodyn. Ther. 26, 193–198 (2019).
L. M. Giroldo, M. P. Felipe, M. A. de Oliveira, E. Munin, L. P. Alves, and M. S. Costa, “Photodynamic antimicrobial chemotherapy (PACT) with methylene blue increases membrane permeability in Candida albicans,” Lasers Med. Sci. 24, 109–112 (2009).
R. C. Souza, J. C. Junqueira, R. D. Rossoni, C. A. Pereira, E. Munin, and A. O. C. Jorge, “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 (2010).
Y. M. Pupo et al., “Susceptibility of Candida albicans to photodynamic therapy using methylene blue and toluidine blue as photosensitizing dyes.,” Acta Odontol. Latinoam. 24, 188–92 (2011).
L. S. Peloi, R. R. S. Soares, C. E. G. Biondo, V. R. Souza, N. Hioka, and E. Kimura, “Photodynamic effect of light-emitting diode light on cell growth inhibition induced by methylene blue,” J. Biosci. 33, 231–237 (2008).
L.M. Dias, T.M. Ferrisse, K.S. Medeiros, E.M. Cilli and A. C. Pavarina. "Use of Photodynamic Therapy Associated with Antimicrobial Peptides for Bacterial Control: A Systematic Review and Meta-Analysis". Int J Mol Sci 23: 3226 (2022).
V. Pérez-Laguna, I. García-Luque, S. Ballesta, A. Rezusta and Y. Gilaberte. "Photodynamic Therapy Combined with Antibiotics or Antifungals against Microorganisms That Cause Skin and Soft Tissue Infections: A Planktonic and Biofilm Approach to Overcome Resistances". Pharmaceuticals 14: 603 (2021).
S. A. B. de Lapena, M. Terra-Garcia, R. A. da C. Ward, R. D. Rossoni, V. M. M. Melo, and J. C. Junqueira, “Enhancing effect of chitosan on methylene blue-mediated photodynamic therapy against C. albicans: A study in planktonic growth, biofilms, and persister cells,” Photodiagnosis Photodyn. Ther. 38, 102837 (2022).
Q. Cai, L. Yang, J. Chen, H. Yang, Z. Gao, and X. Wang, “Successful Sequential Treatment with Itraconazole and ALA-PDT for Cutaneous Granuloma by Candida albicans: A Case Report and Literature Review,” Mycopathologia 183, 829–834 (2018).
L. R. Ferreira et al., “Antimicrobial photodynamic therapy on Candida albicans pre-treated by fluconazole delayed yeast inactivation,” Photodiagnosis Photodyn. Ther. 15, 25–27 (2016).
Y.-H. Hsieh et al., “An in Vitro Study on the Effect of Combined Treatment with Photodynamic and Chemical Therapies on Candida albicans,” Int. J. Mol. Sci. 19, 337 (2018).
L. M. Dias et al., “The Effect of Sub-Lethal Successive Applications of Photodynamic Therapy on Candida albicans Biofilm Depends on the Photosensitizer,” J. Fungi 9, 111 (2023).
E. D. Quiroga, S. J. Mora, M. G. Alvarez, and E. N. Durantini, “Photodynamic inactivation of Candida albicans by a tetracationic tentacle porphyrin and its analogue without intrinsic charges in presence of fluconazole,” Photodiagnosis Photodyn. Ther. 13, 334–340 (2016).
K. Janeth Rimachi Hidalgo et al., “Antimicrobial Photodynamic Therapy in Combination with Nystatin in the Treatment of Experimental Oral Candidiasis Induced by Candida albicans Resistant to Fluconazole,” Pharmaceuticals 12, 140 (2019).
S. B. Snell, T. H. Foster, and C. G. Haidaris, “Miconazole Induces Fungistasis and Increases Killing of Candida albicans Subjected to Photodynamic Therapy†,” Photochem. Photobiol. 88, 596–603 (2012).
L. J. Tavares, E. D. de Avila, M. I. Klein, B. H. D. Panariello, D. M. P. Spolidório, and A. C. Pavarina, “Antimicrobial photodynamic therapy alone or in combination with antibiotic local administration against biofilms of Fusobacterium nucleatum and Porphyromonas gingivalis,” J. Photochem. Photobiol. B Biol. 188, 135–145 (2018).
L. M. Corrochano, “Light in the Fungal World: From Photoreception to Gene Transcription and Beyond,” Annu. Rev. Genet. 53, 149–170 (2019).
P. Dong et al., “Photoinactivation of Catalase Sensitizes Candida albicans and Candida auris to ROS-Producing Agents and Immune Cells,” Adv. Sci. 9, 2104384 (2022).
J. Zhang et al., “Illumination with 630 nm Red Light Reduces Oxidative Stress and Restores Memory by Photo-Activating Catalase and Formaldehyde Dehydrogenase in SAMP8 Mice,” Antioxid. Redox Signal. 30, 1432–1449 (2019).
S. C. de Souza, J. C. Junqueira, I. Balducci, C. Y. Koga-Ito, E. Munin, and A. O. C. Jorge, “Photosensitization of different Candida species by low power laser light,” J. Photochem. Photobiol. B Biol. 83, 34–38 (2006).