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Cold Atmospheric Pressure Plasma Jet Reduces Trichophyton rubrum Adherence and Infection Capacity

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Abstract

This study aimed to evaluate the effects of cold atmospheric pressure plasma (CAPP) jet on Trichophyton rubrum growth, germination and adherence to nail. The effects of plasma jet on T. rubrum conidia germination and on mycelial growth were evaluated by in vitro assays. An ex vivo nail infection model was used to evaluate the effects on conidia adherence and infection. Biochemical analyses of nail fragments exposed or not to CAPP were performed by attenuated total reflectance–Fourier transform infrared (ATR–FTIR) spectroscopy. Plasma jet exposure for 10 and 15 min completely inhibited mycelial growth after only one exposure. Fifteen minutes of exposure could reduce conidia germination in suspension. Fungal suspensions exposed to plasma jet for 10 and 15 min were not able to infect nail specimens. These results were corroborated by ATR–FTIR analyses of nail fragments. In conclusion, single exposure to CAPP for 15 min was able to inhibit fungal growth, adherence and infection capacity. The results suggest that cold atmospheric plasma jet can be a promising alternative for the treatment of onychomycoses caused by T. rubrum.

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References

  1. Faway É, Lambert de Rouvroit C, Poumay Y. In vitro models of dermatophyte infection to investigate epidermal barrier alterations. Exp Dermatol. 2018;27(8):915–22.

    Article  PubMed  Google Scholar 

  2. Asz-Sigall D, Tosti A, Arenas R. Tinea unguium: diagnosis and treatment in practice. Mycopathologia. 2017;182(1–2):95–100.

    Article  CAS  PubMed  Google Scholar 

  3. Chabasse D, Pihet M. Onychomycoses due to molds. J Mycol Med. 2014;24(4):261–8.

    Article  CAS  PubMed  Google Scholar 

  4. Gupta AK, Versteeg SG, Shear NH, Piguet V, Tosti A, Piraccini BM. A practical guide to curing onychomycosis: how to maximize cure at the patient, organism, treatment, and environmental level. Am J Clin Dermatol. 2019;20(1):123–33.

    Article  PubMed  Google Scholar 

  5. Nenoff P, Krüger C, Ginter-Hanselmayer G, Tietz HJ. Mycology—an update. Part 1: dermatomycoses: causative agents, epidemiology and pathogenesis. J Dtsch Dermatol Ges. 2014;12(3):188–209; quiz 10, 188–211; quiz 2.

    PubMed  Google Scholar 

  6. Rouzaud C, Hay R, Chosidow O, Dupin N, Puel A, Lortholary O, et al. Severe dermatophytosis and acquired or innate immunodeficiency: a review. J Fungi (Basel). 2015;2(1):4.

    Article  Google Scholar 

  7. Dogra S, Narang T. Emerging atypical and unusual presentations of dermatophytosis in India. Clin Dermatol Rev. 2017;1(3):12–8.

    Article  Google Scholar 

  8. Zhan P, Liu W. The changing face of dermatophytic infections worldwide. Mycopathologia. 2017;182(1–2):77–86.

    Article  PubMed  Google Scholar 

  9. Sei Y. 2011 epidemiological survey of dermatomycoses in Japan. Med Mycol J. 2015;56(4):J129–35.

    Article  CAS  PubMed  Google Scholar 

  10. Silva LB, de Oliveira DB, da Silva BV, de Souza RA, da Silva PR, Ferreira-Paim K, et al. Identification and antifungal susceptibility of fungi isolated from dermatomycoses. J Eur Acad Dermatol Venereol. 2014;28(5):633–40.

    Article  CAS  PubMed  Google Scholar 

  11. Khan Z, Ahmad S, Alfouzan W, Joseph L, Varghese S. Demonstration of adventitious sporulation in Fusarium petroliphilum onychomycosis. Mycopathologia. 2019;184(2):303–8.

    Article  PubMed  Google Scholar 

  12. Gupta AK, Versteeg SG, Shear NH, Piguet V, Tosti A, Piraccini BM. A practical guide to curing onychomycosis: how to maximize cure at the patient, organism, treatment, and environmental level. Am J Clin Dermatol. 2019;20(1):123–33.

    Article  Google Scholar 

  13. Angora KE, Ira-Bonouman A, Vanga-Bosson AH, Konaté A, Kassi FK, Tuo K, et al. Clinical and mycological characteristics of onychomycosis due to Candida at Institut Pasteur of Côte d’Ivoire. J Mycol Med. 2018;28(1):167–72.

    Article  CAS  PubMed  Google Scholar 

  14. Lipner SR. Pharmacotherapy for onychomycosis: new and emerging treatments. Expert Opin Pharmacother. 2019;20(6):725–35.

    Article  PubMed  Google Scholar 

  15. Iwanaga T, Ushigami T, Anzawa K, Mochizuki T. Pathogenic dermatophytes survive in nail lesions during oral terbinafine treatment for Tinea unguium. Mycopathologia. 2017;182(7–8):673–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Laroussi M. Plasma medicine: a brief introduction. Plasma. 2018;1(1):5.

    Article  Google Scholar 

  17. Schröter S, Wijaikhum A, Gibson AR, West A, Davies HL, Minesi N, et al. Chemical kinetics in an atmospheric pressure helium plasma containing humidity. Phys Chem Chem Phys. 2018;20(37):24263–86.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Nishime TMC, Borges AC, Koga-Ito CY, Machida M, Hein LRO, Kostov KG. Non-thermal atmospheric pressure plasma jet applied to inactivation of different microorganisms. Surf Coat Technol. 2017;312:19–24.

    Article  CAS  Google Scholar 

  19. Weltmann K-D, von Woedtke T. Plasma medicine—current state of research and medical application. Plasma Phys Control Fusion. 2017;59(1):14031.

    Article  Google Scholar 

  20. Brun P, Bernabè G, Marchiori C, Scarpa M, Zuin M, Cavazzana R, et al. Antibacterial efficacy and mechanisms of action of low power atmospheric pressure cold plasma: membrane permeability, biofilm penetration and antimicrobial sensitization. J Appl Microbiol. 2018;125(2):398–408.

    Article  CAS  PubMed  Google Scholar 

  21. Borges AC, Nishime TMC, Kostov KG, Lima GDMG, Gontijo AVL, de Carvalho JNMM, et al. Cold atmospheric pressure plasma jet modulates Candida albicans virulence traits. Clin Plasma Med. 2017;7–8:9–15.

    Article  Google Scholar 

  22. Borges AC, Lima GMG, Nishime TMC, Gontijo AVL, Kostov KG, Koga-Ito CY. Amplitude-modulated cold atmospheric pressure plasma jet for treatment of oral candidiasis: in vivo study. PLoS One. 2018;13(6):e0199832.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Heinlin J, Maisch T, Zimmermann JL, Shimizu T, Holzmann T, Simon M, et al. Contact-free inactivation of Trichophyton rubrum and Microsporum canis by cold atmospheric plasma treatment. Future Microbiol. 2013;8(9):1097–106.

    Article  CAS  PubMed  Google Scholar 

  24. Scholtz V, Soušková H, Hubka V, Švarcová M, Julák J. Inactivation of human pathogenic dermatophytes by non-thermal plasma. J Microbiol Methods. 2015;119:53–8.

    Article  CAS  PubMed  Google Scholar 

  25. Shapourzadeh A, Rahimi-Verki N, Atyabi SM, Shams-Ghahfarokhi M, Jahanshiri Z, Irani S, et al. Inhibitory effects of cold atmospheric plasma on the growth, ergosterol biosynthesis, and keratinase activity in Trichophyton rubrum. Arch Biochem Biophys. 2016;608:27–33.

    Article  CAS  PubMed  Google Scholar 

  26. Pereira FO, Mendes JM, Lima IO, Mota KS, Oliveira WA, Lima EEO. Antifungal activity of geraniol and citronellol, two monoterpenes alcohols, against Trichophyton rubrum involves inhibition of ergosterol biosynthesis. Pharm Biol. 2015;53(2):228–34.

    Article  CAS  Google Scholar 

  27. Klämpfl TG, Isbary G, Shimizu T, Li YF, Zimmermann JL, Stolz W, et al. Cold atmospheric air plasma sterilization against spores and other microorganisms of clinical interest. Appl Environ Microbiol. 2012;78(15):5077–82.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Youssef AB, Kallel A, Azaiz Z, Jemel S, Bada N, Chouchen A, et al. Onychomycosis: which fungal species are involved? Experience of the laboratory of parasitology–mycology of the rabta hospital of Tunis. J Mycol Med. 2018;28(4):651–4.

    Article  PubMed  Google Scholar 

  29. Tachibana H, Kumagai N, Tatsumi Y. Fungicidal activity in the presence of keratin as an important factor contributing to in vivo efficacy: a comparison of efinaconazole, tavaborole, and ciclopirox. J Fungi (Basel). 2017;3(4):58.

    Article  Google Scholar 

  30. Lin X, Alspaugh JA, Liu H, Harris S. Fungal morphogenesis. Cold Spring Harb Perspect Med. 2014;5(2):a019679.

    Article  PubMed  Google Scholar 

  31. Tainwala R, Sharma Y. Pathogenesis of dermatophytoses. Indian J Dermatol. 2011;56(3):259–61.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Gupta BS, Jelle B, Gao T. Application of ATR–FTIR spectroscopy to compare the cell materials of wood decay fungi with wood mould fungi. Int J Spectrosc. 2015;2015:7.

    Article  Google Scholar 

  33. De Bruyne S, Speeckaert R, Boelens J, Hayette MP, Speeckaert M, Delanghe J. Infrared spectroscopy as a novel tool to diagnose onychomycosis. Br J Dermatol. 2019;180(3):637–46.

    Article  PubMed  Google Scholar 

  34. Sowa MG, Wang J, Schultz CP, Ahmed MK, Mantsch HH. Infrared spectroscopic investigation of in vivo and ex vivo human nails. Vib Spectrosc. 1995;10(1):49–56.

    Article  CAS  Google Scholar 

  35. Farhan KM, Sastry TP, Mandal AB. Comparative study on secondary structural changes in diabetic and non-diabetic human finger nail specimen by using FTIR spectra. Clin Chim Acta. 2011;412(3–4):386–9.

    Article  CAS  PubMed  Google Scholar 

  36. Bitencourt TA, Macedo C, Franco ME, Assis AF, Komoto TT, Stehling EG, et al. Transcription profile of Trichophyton rubrum conidia grown on keratin reveals the induction of an adhesin-like protein gene with a tandem repeat pattern. BMC Genom. 2016;17:249.

    Article  Google Scholar 

  37. Szeghalmi A, Kaminskyj S, Gough KM. A synchrotron FTIR microspectroscopy investigation of fungal hyphae grown under optimal and stressed conditions. Anal Bioanal Chem. 2007;387(5):1779–89.

    Article  CAS  PubMed  Google Scholar 

  38. Costa-Orlandi CB, Sardi JC, Santos CT, Fusco-Almeida AM, Mendes-Giannini MJ. In vitro characterization of Trichophyton rubrum and T. mentagrophytes biofilms. Biofouling. 2014;30(6):719–27.

    Article  CAS  PubMed  Google Scholar 

  39. Scholtz V, Soušková H, Švarcová M, Kríha V, Živná H, Julák J. Inactivation of dermatophyte infection by nonthermal plasma on animal model. Med Mycol. 2017;55(4):422–8.

    CAS  PubMed  Google Scholar 

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Acknowledgements

Authors are greatful to São Paulo Research Foundation (FAPESP) for the financial support: Grants #2016/07196-6 (CY Koga-Ito); #2015/21989-6 (KG Kostov) and fellowship #2014/02354-7 (AC Borges).

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ACB and TMCN performed experiments, analyzed data and wrote the paper. GDMGL analyzed data. SDMR performed experiments and analyzed data. KGK designed the study and wrote the paper. GPT carried out FTIR analyses and revised the paper. BRCDM performed FTIR analyses. JPBM conducted SEM analyses. CYK designed the study and wrote the paper.

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Correspondence to Cristiane Yumi Koga-Ito.

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Borges, A.C., Nishime, T.M.C., de Moura Rovetta, S. et al. Cold Atmospheric Pressure Plasma Jet Reduces Trichophyton rubrum Adherence and Infection Capacity. Mycopathologia 184, 585–595 (2019). https://doi.org/10.1007/s11046-019-00375-2

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