Advertisement

Mycopathologia

, Volume 182, Issue 1–2, pp 143–167 | Cite as

Natural Products: An Alternative to Conventional Therapy for Dermatophytosis?

  • Graciliana Lopes
  • Eugénia Pinto
  • Lígia Salgueiro
Article

Abstract

The increased incidence of fungal infections, associated with the widespread use of antifungal drugs, has resulted in the development of resistance, making it necessary to discover new therapeutic alternatives. Among fungal infections, dermatophytoses constitute a serious public health problem, affecting 20–25 % of the world population. Medicinal plants represent an endless source of bioactive molecules, and their volatile and non-volatile extracts are clearly recognized for being the historical basis of therapeutic health care. Because of this, the research on natural products with antifungal activity against dermatophytes has considerably increased in recent years. However, despite the recognized anti-dermatophytic potential of natural products, often advantageous face to commercial drugs, there is still a long way to go until their use in therapeutics. This review attempts to summarize the current status of anti-dermatophytic natural products, focusing on their mechanism of action, the developed pharmaceutical formulations and their effectiveness in human and animal models of infection.

Keywords

Natural products Dermatophytosis Non-volatile extracts Essential oils 

References

  1. 1.
    Richardson MD, Warnock DW. Fungal infection: diagnosis and management. 4th ed. Oxford: Wiley-Blackwell; 2012.CrossRefGoogle Scholar
  2. 2.
    Ghannoum MA, Rice LB. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev. 1999;12:501–17.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Lopes G, Pinto E, Andrade PB, Valentão P. Antifungal activity of phlorotannins against dermatophytes and yeasts: approaches to the mechanism of action and influence on Candida albicans virulence factor. PLoS ONE. 2013;8(8):e72203.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Sharma R, Malik A. Activity of natural products derived essential oils against dermatophytes. WJPPS. 2015;4:1203–9.Google Scholar
  5. 5.
    Soares LA, de Cássia Orlandi Sardi J, Gullo FP, et al. Anti dermatophytic therapy: prospects for the discovery of new drugs from natural products. Braz J Microbiol. 2013;44:1035–41.PubMedCrossRefGoogle Scholar
  6. 6.
    Dhayanithi N, Kumar TA, Kalaiselvam M, Balasubramanian T, Sivakumar N. Anti-dermatophytic activity of marine sponge, Sigmadocia carnosa (Dendy) on clinically isolated fungi. Asian Pac J Trop Biomed. 2012;2:635–9.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Negri M, Salci TP, Shinobu-Mesquita CS, et al. Early state research on antifungal natural products. Molecules. 2014;19:2925–56.PubMedCrossRefGoogle Scholar
  8. 8.
    Gowhar O, Singh NN, Sultan S, et al. Natural herbs as alternative to synthetic antifungal drugs-the future challenging therapy. Br Biomed Bull. 2015;3:440–52.Google Scholar
  9. 9.
    Pinto E, Pina-Vaz C, Salgueiro L, et al. Antifungal activity of the essential oil of Thymus pulegioides on Candida, Aspergillus and dermatophyte species. J Med Microbiol. 2006;55:1367–73.PubMedCrossRefGoogle Scholar
  10. 10.
    Havlickova B, Czaika VA, Friedrich M. Epidemiological trends in skin mycoses worldwide. Mycoses. 2008;51:2–15.PubMedCrossRefGoogle Scholar
  11. 11.
    Drake LA, Patrick DL, Fleckman P, et al. The impact of onychomycosis on quality of life: development of an international onychomycosis-specific questionnaire to measure patient quality of life. J Am Acad Dermatol. 1999;41:189–96.PubMedCrossRefGoogle Scholar
  12. 12.
    Vermout S, Tabart J, Baldo A, et al. Pathogenesis of dermatophytosis. Mycopathologia. 2008;166:267–75.PubMedCrossRefGoogle Scholar
  13. 13.
    Fidel PL, Huffnagle GB. Fungal immunology: from an organ perspective. New-York: Springer; 2006.Google Scholar
  14. 14.
    Weitzman I, Summerbell RC. The dermatophytes. Clin Microbiol Rev. 1995;8:240–59.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Wu L-C, Sun P-L, Chang Y-T. Extensive deep dermatophytosis cause by Trichophyton rubrum in a patient with liver cirrhosis and chronic renal failure. Mycopathologia. 2013;176:457–62.PubMedCrossRefGoogle Scholar
  16. 16.
    Marconi VC, Kradin R, Marty FM, Hospenthal DR, Kotton CN. Disseminated dermatophytosis in a patient with hereditary hemochromatosis and hepatic cirrhosis: case report and review of the literature. Med Mycol. 2010;48:518–27.PubMedCrossRefGoogle Scholar
  17. 17.
    Seebacher C, Bouchara J-P, Mignon B. Updates on the epidemiology of dermatophyte infections. Mycopathologia. 2008;166:335–52.PubMedCrossRefGoogle Scholar
  18. 18.
    Putignani L, D’Arezzo S, Paglia MG, Visca P. DNA-based detection of human pathogenic fungi: dermatophytes, opportunists, and causative agents of deep mycoses. In: Gherbawy Y, Voigt K, Ferenczy L, editors. Molecular identification of fungi. New-York: Springer; 2010. p. 357–415.CrossRefGoogle Scholar
  19. 19.
    White TC, Marr KA, Bowden RA. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev. 1998;11:382–402.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Lorian V. Antibiotics in laboratory medicine. 5th ed. Philadelphia: Lippincott Williams & Wilkins; 2005.Google Scholar
  21. 21.
    Hector RF. Compounds active against cell walls of medically important fungi. Clin Microbiol Rev. 1993;6:1–21.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Li J, Li L, Tian Y, Niu G, Tan H. Hybrid antibiotics with the nikkomycin nucleoside and polyoxin peptidyl moieties. Metab Eng. 2011;13:336–44.PubMedCrossRefGoogle Scholar
  23. 23.
    Gupta AK, Cooper EA. Update in antifungal therapy of dermatophytosis. Mycopathologia. 2008;166:353–67.PubMedCrossRefGoogle Scholar
  24. 24.
    Ortholand J-Y, Ganesan A. Natural products and combinatorial chemistry: back to the future. Curr Opin Chem Biol. 2004;8:271–80.PubMedCrossRefGoogle Scholar
  25. 25.
    Newman DJ, Cragg GM, Snader KM. Natural products as sources of new drugs over the period 1981–2002. J Nat Prod. 2003;66:1022–37.PubMedCrossRefGoogle Scholar
  26. 26.
    Di Santo R. Natural products as antifungal agents against clinically relevant pathogens. Nat Prod Rep. 2010;27:1084–98.PubMedCrossRefGoogle Scholar
  27. 27.
    Houghton P, Raman A. Laboratory handbook for the fractionation of natural extracts. Boston: Springer; 2012.Google Scholar
  28. 28.
    Hostettmann K, Wolfender J-L, Terreaux C. Modern screening techniques for plant extracts. Pharm Biol. 2001;39:18–32.PubMedGoogle Scholar
  29. 29.
    Cheung RCF, Wong JH, Pan WL, et al. Antifungal and antiviral products of marine organisms. Appl Microbiol Biotechnol. 2014;98:3475–94.PubMedCrossRefGoogle Scholar
  30. 30.
    Cardozo KH, Guaratini T, Barros MP, et al. Metabolites from algae with economical impact. Comp Biochem Physiol C: Toxicol Pharmacol. 2007;146:60–78.CrossRefGoogle Scholar
  31. 31.
    Barros MP, Pinto E, Sigaud-Kutner TC, Cardozo KH, Colepicolo P. Rhythmicity and oxidative/nitrosative stress in algae. Biol Rhythm Res. 2005;36:67–82.CrossRefGoogle Scholar
  32. 32.
    Javed I. Antidermatophytic activity of angiospermic plants: a review. Asian J Pharm Clin Res. 2015;8:75–80.Google Scholar
  33. 33.
    Svetaz L, Zuljan F, Derita M, et al. Value of the ethnomedical information for the discovery of plants with antifungal properties. A survey among seven Latin American countries. J Ethnopharmacol. 2010;127:137–58.PubMedCrossRefGoogle Scholar
  34. 34.
    Webster D, Taschereau P, Belland RJ, Sand C, Rennie RP. Antifungal activity of medicinal plant extracts; preliminary screening studies. J Ethnopharmacol. 2008;115:140–6.PubMedCrossRefGoogle Scholar
  35. 35.
    Ali-Shtayeh M, Abu Ghdeib SI. Antifungal activity of plant extracts against dermatophytes. Mycoses. 1999;42:665–72.PubMedCrossRefGoogle Scholar
  36. 36.
    El-Wahidi M, El-Amraoui B, Biard J-F, et al. Variation saisonnière et géographique de l’activité antifongique des extraits de deux éponges marines récoltées sur le littoral atlantique d’El Jadida, Maroc. J Mycol Med. 2011;21:28–32.PubMedCrossRefGoogle Scholar
  37. 37.
    Kuiate J-R, Bessière JM, Zollo PHA, Kuate SP. Chemical composition and antidermatophytic properties of volatile fractions of hexanic extract from leaves of Cupressus lusitanica Mill. from Cameroon. J Ethnopharmacol. 2006;103:160–5.PubMedCrossRefGoogle Scholar
  38. 38.
    Roemer T, Xu D, Singh SB, et al. Confronting the challenges of natural product-based antifungal discovery. Chem Biol. 2011;18:148–64.PubMedCrossRefGoogle Scholar
  39. 39.
    Newman DJ, Cragg GM. Natural products as sources of new drugs over the last 25 years. J Nat Prod. 2007;70:461–77.PubMedCrossRefGoogle Scholar
  40. 40.
    Cragg GM, Newman DJ. Natural products: a continuing source of novel drug leads. BBA Gen Subj. 2013;1830:3670–95.CrossRefGoogle Scholar
  41. 41.
    Vermerris W, Nicholson R (editors). Families of phenolic compounds and means of classification. In: Phenolic compound biochemistry. Netherlands: Springer; 2008. p. 1–34.Google Scholar
  42. 42.
    Bruneton J. Pharmacognosy, phytochemistry, medicinal plants. 2nd ed. Paris: Lavoisier Publishing; 2008.Google Scholar
  43. 43.
    Ayres DC, Loike JD. Lignans: chemical, biological and clinical properties. Cambridge: Cambridge University Press; 1990.CrossRefGoogle Scholar
  44. 44.
    Zacchino S, Rodrıguez G, Santecchia C, et al. In vitro studies on mode of action of antifungal 8.O.4′-neolignans occurring in certain species of Virola and related genera of Myristicaceae. J Ethnopharmacol. 1998;62:35–41.PubMedCrossRefGoogle Scholar
  45. 45.
    Apers S, Vlietinck A, Pieters L. Lignans and neolignans as lead compounds. Phytochem Rev. 2003;2:201–17.CrossRefGoogle Scholar
  46. 46.
    Zacchino SA, López SN, Pezzenati GD, et al. In vitro evaluation of antifungal properties of phenylpropanoids and related compounds acting against dermatophytes. J Nat Prod. 1999;62:1353–7.PubMedCrossRefGoogle Scholar
  47. 47.
    MacRae WD, Towers GN. Biological activities of lignans. Phytochemistry. 1984;23:1207–20.CrossRefGoogle Scholar
  48. 48.
    Freixa B, Vila R, Ferro EA, Adzet T, Cañigueral S. Antifungal principles from Piper fulvescens. Planta Med. 2001;67:873–5.PubMedCrossRefGoogle Scholar
  49. 49.
    Koroishi AM, Foss SR, Cortez DA, et al. In vitro antifungal activity of extracts and neolignans from Piper regnellii against dermatophytes. J Ethnopharmacol. 2008;117:270–7.PubMedCrossRefGoogle Scholar
  50. 50.
    Kurdelas RR, Lima B, Tapia A, et al. Antifungal activity of extracts and prenylated coumarins isolated from Baccharis darwinii Hook & Arn. (Asteraceae). Molecules. 2010;15:4898–907.PubMedCrossRefGoogle Scholar
  51. 51.
    Houghton P, Ismail K, Maxia L, Appendino G. Antidermatophytic prenylated coumarins from asafetida. Planta Med. 2006;72:S008.Google Scholar
  52. 52.
    Stein AC, Sortino M, Avancini C, Zacchino S, von Poser G. Ethnoveterinary medicine in the search for antimicrobial agents: antifungal activity of some species of Pterocaulon (Asteraceae). J Ethnopharmacol. 2005;99:211–4.PubMedCrossRefGoogle Scholar
  53. 53.
    Vera N, Bardón A, Catalan CA, Gedris TE, Herz W. New coumarins from Pterocaulon polystachyum. Planta Med. 2001;67:674–7.PubMedCrossRefGoogle Scholar
  54. 54.
    Mercer DK, Robertson J, Wright K, et al. A prodrug approach to the use of coumarins as potential therapeutics for superficial mycoses. PLoS ONE. 2013;8(11):e80760.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Stewart C. Use of coumarin derivatives in antifungal therapy. U.S. Patent Application No. 12/303,958, 2007.Google Scholar
  56. 56.
    Kostova I. Synthetic and natural coumarins as cytotoxic agents. Curr Med Chem Anticancer Agents. 2005;5:29–46.PubMedCrossRefGoogle Scholar
  57. 57.
    Agüero MB, Svetaz L, Baroni V, et al. Urban propolis from San Juan province (Argentina): ethnopharmacological uses and antifungal activity against Candida and dermatophytes. Ind Crops Prod. 2014;57:166–73.CrossRefGoogle Scholar
  58. 58.
    De Campos MP, Cechinel Filho V, Da Silva RZ, et al. Evaluation of antifungal activity of Piper solmsianum C. DC. var. solmsianum (Piperaceae). Biol Pharm Bull. 2005;28:1527–30.PubMedCrossRefGoogle Scholar
  59. 59.
    Alvarez M, Debattista N, Pappano N. Antimicrobial activity and synergism of some substituted flavonoids. Folia Microbiol. 2008;53:23–8.CrossRefGoogle Scholar
  60. 60.
    Bitencourt TA, TakahasiKomoto T, Marins M, Fachin AL. Antifungal activity of flavonoids and modulation of expression of genes of fatty acid synthesis in the dermatophyte Trichophyton rubrum. BMC Proc. 2014;8(Suppl 4):P53.PubMedCentralCrossRefGoogle Scholar
  61. 61.
    Ghani SBA, Weaver L, Zidan ZH, et al. Microwave-assisted synthesis and antimicrobial activities of flavonoid derivatives. Bioorg Med Chem Lett. 2008;18:518–22.PubMedCrossRefGoogle Scholar
  62. 62.
    Bhadauria S, Kumar P. Broad spectrum antidermatophytic drug for the control of tinea infection in human beings. Mycoses. 2012;55:339–43.PubMedCrossRefGoogle Scholar
  63. 63.
    de Pinho BR. Naphthoquinones and ubiquinone analogues biological properties: modulation of immune and neurological systems. Ph.D. Thesis, Phytochemistry and Pharmacognosy Speciality, Faculty of Pharmacy, University of Porto, Porto, Portugal, 2014.Google Scholar
  64. 64.
    Errante G, La Motta G, Lagana C, et al. Synthesis and evaluation of antifungal activity of naphthoquinone derivatives. Eur J Med Chem. 2006;41:773–8.PubMedCrossRefGoogle Scholar
  65. 65.
    Ryu C-K, Kang H-Y, Yi Y-J, Shin K-H, Lee B-H. Synthesis and antifungal activities of 5/6-arylamino-4,7-dioxobenzothiazoles. Bioorg Med Chem Lett. 2000;10:1589–91.PubMedCrossRefGoogle Scholar
  66. 66.
    Gershon H, Shanks L. Fungitoxicity of 1,4-naphthoquinones to Candida albicans and Trichophyton mentagrophytes. Can J Microbiol. 1975;21:1317–21.PubMedCrossRefGoogle Scholar
  67. 67.
    Dzoyem JP, Tangmouo JG, Kechia FA, et al. In vitro antidermatophytic activity of Diospyros crassiflora Hiern (Ebenaceae). Sudan J Dermatol. 2006;4:10–5.Google Scholar
  68. 68.
    Gupta D, Thappa DM. Dermatoses due to indian cultural practices. Indian J Dermatol. 2015;60:3–12.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Guiraud P, Steiman R, Campos-Takaki G-M, Seigle-Murandi F, Simeon de Buochberg M. Comparison of antibacterial and antifungal activities of lapachol and beta-lapachone. Planta Med. 1994;60:373–4.PubMedCrossRefGoogle Scholar
  70. 70.
    Lown JW. The mechanism of action of quinone antibiotics. Mol Cell Biochem. 1983;55:17–40.PubMedCrossRefGoogle Scholar
  71. 71.
    Lopes GLL. Seaweeds from the Portuguese coast: chemistry, antimicrobial and antiinflammatory capacity. Ph.D. Thesis, Phytochemistry and Pharmacognosy Speciality, Faculty of Pharmacy, University of Porto, Porto, Portugal, 2014.Google Scholar
  72. 72.
    Scalbert A. Antimicrobial properties of tannins. Phytochemistry. 1991;30:3875–83.CrossRefGoogle Scholar
  73. 73.
    Lipińska L, Klewicka E, Sójka M. The structure, occurrence and biological activity of ellagitannins: a general review. Acta Sci Pol Technol Aliment. 2014;13:289–99.PubMedCrossRefGoogle Scholar
  74. 74.
    Foss SR, Nakamura CV, Ueda-Nakamura T, et al. Antifungal activity of pomegranate peel extract and isolated compound punicalagin against dermatophytes. Ann Clin Microbiol Antimicrob. 2014;13:1–6.CrossRefGoogle Scholar
  75. 75.
    Lee MH, Lee KB, Oh SM, Lee BH, Chee HY. Antifungal activities of dieckol isolated from the marine brown alga Ecklonia cava against Trichophyton rubrum. J Korean Soc Appl Biol Chem. 2010;53:504–7.CrossRefGoogle Scholar
  76. 76.
    Koivikko R, Loponen J, Pihlaja K, Jormalainen V. High-performance liquid chromatographic analysis of phlorotannins from the brown alga Fucus vesiculosus. Phytochem Anal. 2007;18:326–32.PubMedCrossRefGoogle Scholar
  77. 77.
    Cordell GA. The alkaloids chemistry and biology, vol. 67. London: Academic Press; 2009.Google Scholar
  78. 78.
    Singh U, Sarma B, Mishra P, Ray A. Antifungal activity of venenatine, an indole alkaloid isolated from Alstonia venenata. Folia Microbiol. 2000;45:173–6.CrossRefGoogle Scholar
  79. 79.
    Emile A, Waikedre J, Herrenknecht C, et al. Bioassay-guided isolation of antifungal alkaloids from Melochia odorata. Phytother Res. 2007;21:398–400.PubMedCrossRefGoogle Scholar
  80. 80.
    Meng F, Zuo G, Hao X, et al. Antifungal activity of the benzo [c] phenanthridine alkaloids from Chelidonium majus Linn against resistant clinical yeast isolates. J Ethnopharmacol. 2009;125:494–6.PubMedCrossRefGoogle Scholar
  81. 81.
    Lohombo-Ekomba M, Okusa P, Penge O, et al. Antibacterial, antifungal, antiplasmodial, and cytotoxic activities of Albertisia villosa. J Ethnopharmacol. 2004;93:331–5.PubMedCrossRefGoogle Scholar
  82. 82.
    Ferheen S, Ahmed E, Afza N, et al. Haloxylines A and B, antifungal and cholinesterase inhibiting piperidine alkaloids from Haloxylon salicornicum. Chem Pharm Bull. 2005;53:570–2.PubMedCrossRefGoogle Scholar
  83. 83.
    Xiao C, Ji Q, Rajput Z, et al. Antifungal efficacy of Phellodendron amurense ethanol extract against Trichophyton mentagrophytes in rabbits. Pak Vet J. 2014;34:219–23.Google Scholar
  84. 84.
    Sher A. Antimicrobial activity of natural products from medicinal plants. Gomal J Med Sci. 2004;7:72–8.Google Scholar
  85. 85.
    Vincken J-P, Heng L, de Groot A, Gruppen H. Saponins, classification and occurrence in the plant kingdom. Phytochemistry. 2007;68:275–97.PubMedCrossRefGoogle Scholar
  86. 86.
    Houghton P, Patel N, Jurzysta M, Biely Z, Cheung C. Antidermatophyte activity of medicago extracts and contained saponins and their structure-activity relationships. Phytother Res. 2006;20:1061–6.PubMedCrossRefGoogle Scholar
  87. 87.
    Njateng GSS, Du Z, Gatsing D, et al. Antifungal properties of a new terpernoid saponin and other compounds from the stem bark of Polyscias fulva Hiern (Araliaceae). BMC Complement Altern Med. 2015;15:1–12.CrossRefGoogle Scholar
  88. 88.
    Lunga PK, Qin X-J, Yang XW, et al. Antimicrobial steroidal saponin and oleanane-type triterpenoid saponins from Paullinia pinnata. BMC Complement Altern Med. 2014;14:1–7.CrossRefGoogle Scholar
  89. 89.
    Avis T. Antifungal compounds that target fungal membranes: applications in plant disease control. Can J Plant Pathol. 2007;29:323–9.CrossRefGoogle Scholar
  90. 90.
    Kandi S, Godishala V, Rao P, Ramana K. Biomedical significance of terpenes: an insight. Biomed Biotechnol. 2015;3:8–10.Google Scholar
  91. 91.
    Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils—a review. Food Chem Toxicol. 2008;46:446–75.PubMedCrossRefGoogle Scholar
  92. 92.
    Baser KHC, Demirci F. Chemistry of essential oils. In: Berger RG, editor. Flavours and fragrances—chemistry, bioprocessing and sustainability. Springer: Berlin; 2007. p. 43–86.Google Scholar
  93. 93.
    Theis N, Lerdau M. The evolution of function in plant secondary metabolites. Int J Plant Sci. 2003;164:93–102.CrossRefGoogle Scholar
  94. 94.
    Zuzarte M, Gonçalves M, Canhoto J, Salgueiro L. Antidermatophytic activity of essential oils. In: Méndez-Vilas A, editor. Science against microbial pathogens: communicating current research and technological advances. Singapore: World Scientific; 2011. p. 1167–78.Google Scholar
  95. 95.
    Smith R, Cohen S, Doull J, et al. A procedure for the safety evaluation of natural flavor complexes used as ingredients in food: essential oils. Food Chem Toxicol. 2005;43:345–63.PubMedCrossRefGoogle Scholar
  96. 96.
    Masotti V, Juteau F, Bessière JM, Viano J. Seasonal and phenological variations of the essential oil from the narrow endemic species Artemisia molinieri and its biological activities. J Agric Food Chem. 2003;51:7115–21.PubMedCrossRefGoogle Scholar
  97. 97.
    Lawrence BM. A planning scheme to evaluate new aromatic plants for the flavor and fragrance industries. In: Janick J, Simon JE, editors. New crops. New York: Wiley; 1993. p. 620–7.Google Scholar
  98. 98.
    Edris AE. Pharmaceutical and therapeutic potentials of essential oils and their individual volatile constituents: a review. Phytother Res. 2007;21:308–23.PubMedCrossRefGoogle Scholar
  99. 99.
    Maruzzella JC, Liguori L. The in vitro antifungal activity of essential oils. J Am Pharm Assoc. 1958;47:250–4.CrossRefGoogle Scholar
  100. 100.
    Maxia A, Falconieri D, Piras A, et al. Chemical composition and antifungal activity of essential oils and supercritical CO2 extracts of Apium nodiflorum (L.) Lag. Mycopathologia. 2012;174:61–7.PubMedCrossRefGoogle Scholar
  101. 101.
    Marongiu B, Piras A, Porcedda S, et al. Isolation of the volatile fraction from Apium graveolens L. (Apiaceae) by supercritical carbon dioxide extraction and hydrodistillation: chemical composition and antifungal activity. Nat Prod Res. 2013;27:1521–7.PubMedCrossRefGoogle Scholar
  102. 102.
    Valente J, Resende R, Zuzarte M, et al. Bioactivity and safety profile of Daucus carota subsp. maximus essential oil. Ind Crops Prod. 2015;77:218–24.CrossRefGoogle Scholar
  103. 103.
    Valente J, Zuzarte M, Resende R, et al. Daucus carota subsp. gummifer essential oil as a natural source of antifungal and anti-inflammatory drugs. Ind Crops Prod. 2015;65:361–6.CrossRefGoogle Scholar
  104. 104.
    Cavaleiro C, Gonçalves MJ, Serra D, et al. Composition of a volatile extract of Eryngium duriaei subsp. juresianum (M. Laínz) M. Laínz, signalised by the antifungal activity. J Pharm Biomed Anal. 2011;54:619–22.PubMedCrossRefGoogle Scholar
  105. 105.
    Flores FC, Beck RC, da Silva Cde B. Essential oils for treatment for onychomycosis: a mini-review. Mycopathologia. 2016;181:9–15.PubMedCrossRefGoogle Scholar
  106. 106.
    Zuzarte M, Gonçalves MJ, Cavaleiro C, et al. Chemical composition and antifungal activity of the essential oils of Lavandula pedunculata (Miller) Cav. Chem Biodivers. 2009;6:1283–92.PubMedCrossRefGoogle Scholar
  107. 107.
    Zuzarte M, Gonçalves MJ, Cavaleiro C, et al. Chemical composition and antifungal activity of the essential oils of Lavandula viridis L’Hér. J Med Microbiol. 2011;60:612–8.PubMedCrossRefGoogle Scholar
  108. 108.
    Tullio V, Nostro A, Mandras N, et al. Antifungal activity of essential oils against filamentous fungi determined by broth microdilution and vapour contact methods. J Appl Microbiol. 2007;102:1544–50.PubMedCrossRefGoogle Scholar
  109. 109.
    I J, Karim Moharam BA, Santhanam J, Jamal JA. Correlation between chemical composition and antifungal activity of the essential oils of eight Cinnamomum species. Pharm Biol. 2008;46:406–12.CrossRefGoogle Scholar
  110. 110.
    Elaissi A, Rouis Z, Salem NAB, et al. Chemical composition of 8 eucalyptus species’ essential oils and the evaluation of their antibacterial, antifungal and antiviral activities. BMC Complement Altern Med. 2012;12:1–15.CrossRefGoogle Scholar
  111. 111.
    Kavoosi G, Rowshan V. Chemical composition, antioxidant and antimicrobial activities of essential oil obtained from Ferula assa-foetida oleo-gum-resin: effect of collection time. Food Chem. 2013;138:2180–7.PubMedCrossRefGoogle Scholar
  112. 112.
    Marongiu B, Maxia A, Piras A, et al. Isolation of Crithmum maritimum L. volatile oil by supercritical carbon dioxide extraction and biological assays. Nat Prod Res. 2007;21:1145–50.PubMedCrossRefGoogle Scholar
  113. 113.
    Vale-Silva L, Silva M-J, Oliveira D, et al. Correlation of the chemical composition of essential oils from Origanum vulgare subsp. virens with their in vitro activity against pathogenic yeasts and filamentous fungi. J Med Microbiol. 2012;61:252–60.PubMedCrossRefGoogle Scholar
  114. 114.
    Pinto E, Vale-Silva L, Cavaleiro C, Salgueiro L. Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J Med Microbiol. 2009;58:1454–62.PubMedCrossRefGoogle Scholar
  115. 115.
    Miron D, Battisti F, Silva FK, et al. Antifungal activity and mechanism of action of monoterpenes against dermatophytes and yeasts. Rev Bras Farmacogn. 2014;24:660–7.CrossRefGoogle Scholar
  116. 116.
    Miron D, Cornelio R, Troleis J, et al. Influence of penetration enhancers and molecular weight in antifungals permeation through bovine hoof membranes and prediction of efficacy in human nails. Eur J Pharm Sci. 2014;51:20–5.PubMedCrossRefGoogle Scholar
  117. 117.
    De Lucca AJ, Pauli A, Schilcher H, et al. Fungicidal and bactericidal properties of bisabolol and dragosantol. J Essent Oil Res. 2011;23:47–54.CrossRefGoogle Scholar
  118. 118.
    Pinto E, Hrimpeng K, Lopes G, et al. Antifungal activity of Ferulago capillaris essential oil against Candida, Cryptococcus, Aspergillus and dermatophyte species. Eur J Clin Microbiol Infect Dis. 2013;32:1311–20.PubMedCrossRefGoogle Scholar
  119. 119.
    Shin S, Lim S. Antifungal effects of herbal essential oils alone and in combination with ketoconazole against Trichophyton spp. J Appl Microbiol. 2004;97:1289–96.PubMedCrossRefGoogle Scholar
  120. 120.
    Pyun M-S, Shin S. Antifungal effects of the volatile oils from Allium plants against Trichophyton species and synergism of the oils with ketoconazole. Phytomedicine. 2006;13:394–400.PubMedCrossRefGoogle Scholar
  121. 121.
    Khan MSA, Ahmad I. Antifungal activity of essential oils and their synergy with fluconazole against drug-resistant strains of Aspergillus fumigatus and Trichophyton rubrum. Appl Microbiol Biotechnol. 2011;90:1083–94.PubMedCrossRefGoogle Scholar
  122. 122.
    Houël E, Rodrigues A, Jahn-Oyac A, et al. In vitro antidermatophytic activity of Otacanthus azureus (Linden) Ronse essential oil alone and in combination with azoles. J Appl Microbiol. 2014;116:288–94.PubMedCrossRefGoogle Scholar
  123. 123.
    Pina-Vaz C, Gonçalves Rodrigues A, Pinto E, et al. Antifungal activity of Thymus oils and their major compounds. J Eur Acad Dermatol Venereol. 2004;18:73–8.PubMedCrossRefGoogle Scholar
  124. 124.
    Lazutka J, Mierauskien J, Slapšyt G, Dedonyt V. Genotoxicity of dill (Anethum graveolens L.), peppermint (Mentha × piperita L.) and pine (Pinus sylvestris L.) essential oils in human lymphocytes and Drosophila melanogaster. Food Chem Toxicol. 2001;39:485–92.PubMedCrossRefGoogle Scholar
  125. 125.
    Andersen PH, Jensen NJ. Mutagenic investigation of peppermint oil in the Salmonella/mammalian-microsome test. Mutat Res Genet Toxicol. 1984;138:17–20.CrossRefGoogle Scholar
  126. 126.
    Hasheminejad G, Caldwell J. Genotoxicity of the alkenylbenzenes α- and β-asarone, myristicin and elemicin as determined by the UDS assay in cultured rat hepatocytes. Food Chem Toxicol. 1994;32:223–31.PubMedCrossRefGoogle Scholar
  127. 127.
    Abel G. Chromosome-damaging effect of beta-asaron on human lymphocytes. Planta Med. 1987;53:251–3.PubMedCrossRefGoogle Scholar
  128. 128.
    Morales-Ramirez P, Madrigal-Bujaidar E, Mercader-Martinez J, et al. Sister-chromatid exchange induction produced by in vivo and in vitro exposure to alpha-asarone. Mutat Res Genet Toxicol. 1992;279:269–73.CrossRefGoogle Scholar
  129. 129.
    Kim S, Liem A, Stewart B, Miller J. New studies on trans-anethole oxide and trans-asarone oxide. Carcinogenesis. 1999;20:1303–7.PubMedCrossRefGoogle Scholar
  130. 130.
    Gomes-Carneiro MR, Felzenszwalb I, Paumgartten FJ. Mutagenicity testing of (±)-camphor, 1,8-cineole, citral, citronellal, (−)-menthol and terpineol with the Salmonella/microsome assay. Mutat Res, Genet Toxicol Environ Mutagen. 1998;416:129–36.CrossRefGoogle Scholar
  131. 131.
    Stammati A, Bonsi P, Zucco F, et al. Toxicity of selected plant volatiles in microbial and mammalian short-term assays. Food Chem Toxicol. 1999;37:813–23.PubMedCrossRefGoogle Scholar
  132. 132.
    Pinto E, Salgueiro LR, Cavaleiro C, Palmeira A, Gonçalves MJ. In vitro susceptibility of some species of yeasts and filamentous fungi to essential oils of Salvia officinalis. Ind Crops Prod. 2007;26:135–41.CrossRefGoogle Scholar
  133. 133.
    Inouye S, Nishiyama Y, Uchida K, et al. The vapor activity of oregano, perilla, tea tree, lavender, clove, and geranium oils against a Trichophyton mentagrophytes in a closed box. J Infect Chemother. 2006;12:349–54.PubMedCrossRefGoogle Scholar
  134. 134.
    Jeung E-B, Choi I-G. Antifungal activities of the essential oils in Syzygium aromaticum (L.) Merr. Et Perry and Leptospermum petersonii Bailey and their constituents against various dermatophytes. J Microbiol. 2007;45:460–5.PubMedGoogle Scholar
  135. 135.
    Cowan MM. Plant products as antimicrobial agents. Clin Microbiol Rev. 1999;12:564–82.PubMedPubMedCentralGoogle Scholar
  136. 136.
    Bajpai VK, Yoon JI, Kang SC. Antifungal potential of essential oil and various organic extracts of Nandina domestica Thunb. against skin infectious fungal pathogens. Appl Microbiol Biotechnol. 2009;83:1127–33.PubMedCrossRefGoogle Scholar
  137. 137.
    Rana B, Singh U, Taneja V. Antifungal activity and kinetics of inhibition by essential oil isolated from leaves of Aegle marmelos. J Ethnopharmacol. 1997;57:29–34.PubMedCrossRefGoogle Scholar
  138. 138.
    Zacchino S, Santecchia C, López S, et al. In vitro antifungal evaluation and studies on mode of action of eight selected species from the Argentine flora. Phytomedicine. 1998;5:389–95.PubMedCrossRefGoogle Scholar
  139. 139.
    Natarajan V, Venugopal P, Menon T. Effect of Azadirachta indica (neem) on the growth pattern of dermatophytes. Indian J Med Microbiol. 2003;21:98–101.PubMedGoogle Scholar
  140. 140.
    Lopez S, Furlan R, Zacchino S. Detection of antifungal compounds in Polygonum ferrugineum Wedd. extracts by bioassay-guided fractionation. Some evidences of their mode of action. J Ethnopharmacol. 2011;138:633–6.PubMedCrossRefGoogle Scholar
  141. 141.
    Svetaz L, Agüero MB, Alvarez S, et al. Antifungal activity of Zuccagnia punctata Cav.: evidence for the mechanism of action. Planta Med. 2007;73:1074–80.PubMedCrossRefGoogle Scholar
  142. 142.
    Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi, 2nd ed. Approved standard. CLSI document M38-A2. Clinical and Laboratory Standards Institute, Wayne, PA.Google Scholar
  143. 143.
    Nweze E, Mukherjee P, Ghannoum M. Agar-based disk diffusion assay for susceptibility testing of dermatophytes. J Clin Microbiol. 2010;48:3750–2.PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Shehata AS, Mukherjee PK, Ghannoum MA. Comparison between the standardized clinical and laboratory standards institute M38-A2 method and a 2,3-bis (2-methoxy-4-nitro-5-[(sulphenylamino) carbonyl]-2H-tetrazolium hydroxide-based method for testing antifungal susceptibility of dermatophytes. J Clin Microbiol. 2008;46:3668–71.PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Lopes G, Andrade PB, Valentão P. Screening of a marine algal extract for antifungal activities. In: Stengel DB, Connan S, editors. Natural products from marine algae: methods and protocols, methods in molecular biology. New York: Springer Science; 2015. p. 411–20.CrossRefGoogle Scholar
  146. 146.
    Hadacek F, Greger H. Testing of antifungal natural products: methodologies, comparability of results and assay choice. Phytochem Anal. 2000;11:137–47.CrossRefGoogle Scholar
  147. 147.
    Kassem A. Development and formulation of a new natural product for the treatment of pityriasis versicolor and skin dermatophyte infections. Ph.D Thesis, Faculty of Pharmacy, University of Khartoum, Sudan, 2015.Google Scholar
  148. 148.
    Buck DS. Comparison of two topical preparations for the treatment of onychomycosis: Melaleuca altemifilia (tea tree) oil and clotrimazole. J Fam Pract. 1994;38:601–5.PubMedGoogle Scholar
  149. 149.
    Syed T, Qureshi Z, Ali S, Ahmad S, Ahmad S. Treatment of toenail onychomycosis with 2% butenafine and 5% Melaleuca alternifolia (tea tree) oil in cream. Trop Med Int Health. 1999;4:284–7.PubMedCrossRefGoogle Scholar
  150. 150.
    Derby R, Rohal P, Jackson C, Beutler A, Olsen C. Novel treatment of onychomycosis using over-the-counter mentholated ointment: a clinical case series. J Am Board Fam Med. 2011;24:69–74.PubMedCrossRefGoogle Scholar
  151. 151.
    Lee S-J, Han J-I, Lee G-S, et al. Antifungal effect of eugenol and nerolidol against Microsporum gypseum in a guinea pig model. Biol Pharm Bull. 2007;30:184–8.PubMedCrossRefGoogle Scholar
  152. 152.
    Mugnaini L, Nardoni S, Pinto L, et al. In vitro and in vivo antifungal activity of some essential oils against feline isolates of Microsporum canis. J Mycol Med. 2012;22:179–84.PubMedCrossRefGoogle Scholar
  153. 153.
    Wagini NH, Abbas MS, Soliman AS, Hanafy YA. Badawy E-SM. In vitro and in vivo anti dermatophytes activity of Lawsonia inermis L. (henna) leaves against ringworm and its etiological agents. Am. J Clin Exp Med. 2014;2:51–8.CrossRefGoogle Scholar
  154. 154.
    Njateng GSS, Gatsing D, Mouokeu RS, Lunga PK, Kuiate J-R. In vitro and in vivo antidermatophytic activity of the dichloromethane-methanol (1:1 v/v) extract from the stem bark of Polyscias fulva Hiern (Araliaceae). BMC Complement Altern Med. 2013;13:1–10.CrossRefGoogle Scholar
  155. 155.
    Nyong EE, Odeniyi MA, Moody JO. In vitro and in vivo antimicrobial evaluation of alkaloidal extracts of Enantia chlorantha stem bark and their formulated ointments. Acta Pol Pharm. 2015;72:147–52.PubMedGoogle Scholar
  156. 156.
    Singh G, Kumar P, Joshi SC. Treatment of dermatophytosis by a new antifungal agent ‘apigenin’. Mycoses. 2014;57:497–506.PubMedCrossRefGoogle Scholar
  157. 157.
    Romero-Cerecero O, Román-Ramos R, Zamilpa A, et al. Clinical trial to compare the effectiveness of two concentrations of the Ageratina pichinchensis extract in the topical treatment of onychomycosis. J Ethnopharmacol. 2009;126:74–8.PubMedCrossRefGoogle Scholar
  158. 158.
    Bindra RL, Singh AK, Shawl AS, Kumar S. Anti-fungal herbal formulation for treatment of human nails fungus and process thereof. U.S. Patent No. 6,296,838. 2 Oct. 2001.Google Scholar
  159. 159.
    Céspedes CL, Avila JG, Garcıa AM, et al. Antifungal and antibacterial activities of Araucaria araucana (Mol.) K. Koch heartwood lignans. Z Naturforsch C. 2006;61:35–43.PubMedCrossRefGoogle Scholar
  160. 160.
    Ahmad K, Sultana N. Studies on bioassay directed antifungal activity of medicinal plants Calotropis procera, Skimmia laureola, Peltophorum pterocarpum and two pure natural compounds ulopterol and 4-methoxy-1-methyl-3-(2′S-hydroxy-3′-ene butyl)-2-quinolone. J Chem Soc Pak. 2003;25:328–30.Google Scholar
  161. 161.
    Stein AC, Álvarez S, Avancini C, Zacchino S, von Poser G. Antifungal activity of some coumarins obtained from species of Pterocaulon (Asteraceae). J Ethnopharmacol. 2006;107:95–8.PubMedCrossRefGoogle Scholar
  162. 162.
    Navarro-García VM, Rojas G, Avilés M, Fuentes M, Zepeda G. In vitro antifungal activity of coumarin extracted from Loeselia mexicana Brand. Mycoses. 2011;54:569–71.CrossRefGoogle Scholar
  163. 163.
    Sathiamoorthy B, Gupta P, Kumar M, et al. New antifungal flavonoid glycoside from Vitex negundo. Bioorg Med Chem Lett. 2007;17:239–42.PubMedCrossRefGoogle Scholar
  164. 164.
    Mbaveng AT, Ngameni B, Kuete V, et al. Antimicrobial activity of the crude extracts and five flavonoids from the twigs of Dorstenia barteri (Moraceae). J Ethnopharmacol. 2008;116:483–9.PubMedCrossRefGoogle Scholar
  165. 165.
    Prasad NR, Anandi C, Balasubramanian S, Pugalendi K. Antidermatophytic activity of extracts from Psoralea corylifolia (Fabaceae) correlated with the presence of a flavonoid compound. J Ethnopharmacol. 2004;91:21–4.CrossRefGoogle Scholar
  166. 166.
    Zhang H-X, Lunga P-K, Li Z-J, Dai Q, Du Z-Z. Flavonoids and stilbenoids from Derris eriocarpa. Fitoterapia. 2014;95:147–53.PubMedCrossRefGoogle Scholar
  167. 167.
    Singh D, Verma N, Raghuwanshi S, Shukla P, Kulshreshtha D. Antifungal anthraquinones from Saprosma fragrans. Bioorg Med Chem Lett. 2006;16:4512–4.PubMedCrossRefGoogle Scholar
  168. 168.
    Feresin GE, Tapia A, Sortino M, et al. Bioactive alkyl phenols and embelin from Oxalis erythrorhiza. J Ethnopharmacol. 2003;88:241–7.PubMedCrossRefGoogle Scholar
  169. 169.
    Perry NB, Blunt JW, Munro MH. A cytotoxic and antifungal 1,4-naphthoquinone and related compounds from a New Zealand brown alga, Landsburgia quercifolia. J Nat Prod. 1991;54:978–85.PubMedCrossRefGoogle Scholar
  170. 170.
    Singh S, Prasad R, Pathania K, Joshi H. Antifungal activity of plumbagin & isodiospyrin from Diospyros kaki root bark. Asian J Plant Sci Res. 2012;2:1–5.Google Scholar
  171. 171.
    Gozubuyuk G, Aktas E, Yigit N. An ancient plant Lawsonia inermis (henna): determination of in vitro antifungal activity against dermatophytes species. J Mycol Med. 2014;24:313–8.PubMedCrossRefGoogle Scholar
  172. 172.
    Thouvenel C, Gantier JC, Duret P, et al. Antifungal compounds from Zanthoxylum chiloperone var. angustifolium. Phytother Res. 2003;17:678–80.PubMedCrossRefGoogle Scholar
  173. 173.
    Morteza-Semnani K, Amin G, Shidfar M, Hadizadeh H, Shafiee A. Antifungal activity of the methanolic extract and alkaloids of Glaucium oxylobum. Fitoterapia. 2003;74:493–6.PubMedCrossRefGoogle Scholar
  174. 174.
    Chakraborty A, Chowdhury B, Bhattacharyya P. Clausenol and clausenine—two carbazole alkaloids from Clausena anisata. Phytochemistry. 1995;40:295–8.PubMedCrossRefGoogle Scholar
  175. 175.
    Volleková A, Košt’álová D, Kettmann V, Tóth J. Antifungal activity of Mahonia aquifolium extract and its major protoberberine alkaloids. Phytother Res. 2003;17:834–7.PubMedCrossRefGoogle Scholar
  176. 176.
    Duraipandiyan V, Ignacimuthu S. Antibacterial and antifungal activity of flindersine isolated from the traditional medicinal plant, Toddalia asiatica (L.) Lam. J Ethnopharmacol. 2009;123:494–8.PubMedCrossRefGoogle Scholar
  177. 177.
    Escalante AM, Santecchia CB, López SN, et al. Isolation of antifungal saponins from Phytolacca tetramera, an Argentinean species in critic risk. J Ethnopharmacol. 2002;82:29–34.PubMedCrossRefGoogle Scholar
  178. 178.
    Favel A, Kemertelidze E, Benidze M, Fallague K, Regli P. Antifungal activity of steroidal glycosides from Yucca gloriosa L. Phytother Res. 2005;19:158–61.PubMedCrossRefGoogle Scholar
  179. 179.
    Tamura Y, Mizutani K, Ikeda T, et al. Antimicrobial activities of saponins of pericarps of Sapindus mukurossi on dermatophytes. Nat Med. 2001;55:11–6.Google Scholar
  180. 180.
    Stergiopoulou T, De Lucca AJ, Meletiadis J, et al. In vitro activity of CAY-1, a saponin from Capsicum frutescens, against Microsporum and Trichophyton species. Med Mycol. 2008;46:805–10.PubMedCrossRefGoogle Scholar
  181. 181.
    García-Sosa K, Sánchez-Medina A, Álvarez SL, et al. Antifungal activity of sakurasosaponin from the root extract of Jacquinia flammea. Nat Prod Res. 2011;25:1185–9.PubMedCrossRefGoogle Scholar
  182. 182.
    Lopez-Villegas EO, Herrera-Arellano A, de Los Angeles Martinez-Rivera M, et al. Ultrastructural changes on clinical isolates of Trichophyton rubrum, Trichophyton mentagrophytes, and Microsporum gypseum caused by Solanum chrysotrichum saponin SC-2. Planta Med. 2009;75:1517–20.PubMedCrossRefGoogle Scholar
  183. 183.
    Cavaleiro C, Pinto E, Gonçalves M, Salgueiro L. Antifungal activity of Juniperus essential oils against dermatophyte, Aspergillus and Candida strains. J Appl Microbiol. 2006;100:1333–8.PubMedCrossRefGoogle Scholar
  184. 184.
    Salgueiro L, Pinto E, Goncalves M, et al. Chemical composition and antifungal activity of the essential oil of Thymbra capitata. Planta Med. 2004;70:572–5.PubMedCrossRefGoogle Scholar
  185. 185.
    Flach A, Gregel B, Simionatto E, et al. Chemical analysis and antifungal activity of the essential oil of Calea clematidea. Planta Med. 2002;68:836–8.PubMedCrossRefGoogle Scholar
  186. 186.
    Tavares AC, Gonçalves MJ, Cruz MT, et al. Essential oils from Distichoselinum tenuifolium: chemical composition, cytotoxicity, antifungal and anti-inflammatory properties. J Ethnopharmacol. 2010;130:593–8.PubMedCrossRefGoogle Scholar
  187. 187.
    Zuzarte M, Vale-Silva L, Gonçalves M, et al. Antifungal activity of phenolic-rich Lavandula multifida L. essential oil. Eur J Clin Microbiol Infect Dis. 2012;31:1359–66.PubMedCrossRefGoogle Scholar
  188. 188.
    Pinto E, Gonçalves MJ, Oliveira P, et al. Activity of Thymus caespititius essential oil and α-terpineol against yeasts and filamentous fungi. Ind Crops Prod. 2014;62:107–12.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental ResearchUniversity of PortoPortoPortugal
  2. 2.Microbiology Service, Biological Sciences Department, Faculty of PharmacyUniversity of PortoPortoPortugal
  3. 3.CNC.IBILI/Faculty of PharmacyUniversity of CoimbraCoimbraPortugal

Personalised recommendations