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Mycopathologia

, Volume 174, Issue 3, pp 223–232 | Cite as

Antifungal Activities of Different Extracts of Marine Macroalgae Against Dermatophytes and Candida Species

  • Elica Amara Cecilia GuedesEmail author
  • Maria Anilda dos Santos Araújo
  • Aryanna Kelly Pinheiro Souza
  • Larissa Isabela Oliveira de Souza
  • Lurdiana Dayse de Barros
  • Fernanda Cristina de Albuquerque Maranhão
  • Antônio Euzébio Goulart Sant’Ana
Article

Abstract

Algae are bioactive natural resources, and due to the medical importance of superficial mycoses, we focused the action of macroalgae extracts against dermatophytes and Candida species. Seaweed obtained from the Riacho Doce beach, Alagoas (Brazil), were screened for the antifungal activity, through crude extracts using dichloromethane, chloroform, methanol, ethanol, water and chloroform and hexane fractions of green, brown and red algae in assays with standard strains of the dermatophytes Trichophyton rubrum, T. tonsurans, T. mentagrophytes, Microsporum canis, M. gypseum and yeasts Candida albicans, C. krusei, C. guilliermondi and C. parapsilosis. The M44-A and M27-A2/M38A manuals by CLSI were followed, and the minimum inhibitory concentration (MIC) ranged from 0.03 to 16.00 μg ml−1, and an inhibition halo of 10.00–25.00 mm was observed for dermatophytes, while for yeast, it was from 8.00 to 16.00 μg ml−1 and 10.00–15.00 mm. M. canis showed MIC of 0.03 μg ml−1 and the largest inhibition halo in T. rubrum (25.00 mm) through the use of the methanol extract. For C. albicans, dichloromethane, methanol and ethanol extracts formed the largest inhibition halo. The ethanol extract was shown to be the best inhibiting fungi growth, and chloroform and hexane fractions of H. musciformis inhibited the growth of all dermatophytes and C. albicans, yielding the conclusion that apolar extracts obtained from algae presented the best activity against important pathogenic fungi.

Keywords

Dermatophyte Trichophyton Candida Macroalgae Extracts 

Notes

Acknowledgments

We are grateful to Ana Maria Queijeiro Lopes (IQB/UFAL) and Eurípedes Alves Silva Filho (ICBS/UFAL) for suggestions, Júlio César Voltolini for support in statistical analysis and to Abilio Borghi for the English review on the manuscript. This work was supported by grants from the CAPES.

Conflict of interest

There is no conflict of interest in this paper, and all authors agree to publication.

References

  1. 1.
    Peres NTA, Maranhão FCA, Rossi A, Martinez-Rossi NM. Dermatophytes: host pathogen interaction and antifungal resistance. An Bras Dermatol. 2010;85:657–67.PubMedCrossRefGoogle Scholar
  2. 2.
    Hay RJ, Jones RM. New molecular tools in the diagnosis of superficial fungal infections. Clin Dermatol. 2010;4:190–6.CrossRefGoogle Scholar
  3. 3.
    Mota CRA, Miranda KC, Lemos JA, Costa CR, Hasimoto LKS, Passos XS, Meneses HS, Silva MR. Comparison of in vitro activity of five antifungal agents against dermatophytes, using the agar dilution and broth microdilution methods. Rev Soc Bras Med Trop. 2009;42:250–4.PubMedGoogle Scholar
  4. 4.
    Maranhão FC, Paião FG, Martinez-Rossi NM. Isolation of transcripts over-expressed in human pathogen Trichophyton rubrum during growth in keratin. Microbiol Pathog. 2007;43:166–72.CrossRefGoogle Scholar
  5. 5.
    Seebacher C, Bouchara JP, Mignon B. Updates on the epidemiology of dermatophyte infections. Mycopathologia. 2008;166:335–52.PubMedCrossRefGoogle Scholar
  6. 6.
    Williams D, Lewis M. Pathogenesis and treatment of oral candidosis. J Oral Microbiol. 2011;3:5771.Google Scholar
  7. 7.
    Pappas PG, Kauffman CA, Andes D, Benjamin DK, Calandra TF, Edwards JE, Filler SG, Fisher JF, Kullberg BJ, Ostrosky-Zeichner L, Reboli AC, Rex JH, Walsh TJ, Soberl JD. Clinical practice guidelines for the management of candidiasis: 2009 update by the infectious diseases society of american. Clin Infect Dis. 2009;48:503–35.PubMedCrossRefGoogle Scholar
  8. 8.
    Diogo HC, Sarpieri A, Melhem M, Pires MC. Evaluation of the disk-diffusion method to determine the in vitro efficacy of terbinafine against subcutaneous and superficial mycoses agents. An Bras Dermatol. 2010;85:324–30.PubMedCrossRefGoogle Scholar
  9. 9.
    Tresoldi T, Barison EM, Pereira RM, Padoveze MC, Trabasso P. Risk factors associated witch the acquisition of multiresistant bacteria in pediatric nursery. J Pediatr. 2000;4:275–86.Google Scholar
  10. 10.
    Dovigo LN, Pavarina AC, Mima EGO, Giampaolo ET, Vergani CE, Bagnato VS. Fungicidal effect of photodynamic therapy against fluconazole-resistant Candida albicans and Candida glabrata. Mycoses. 2009;54:123–30.CrossRefGoogle Scholar
  11. 11.
    Mishra NN, Prasad T, Sharma N, Payasi A, Prasad R, Gupta DK, Singh R. Pathogenicity and drug resistance in Candida albicans and other yeast species. A review. Acta Microbiol Immunol Hung. 2007;54:201–35.PubMedCrossRefGoogle Scholar
  12. 12.
    Rizvi MA, Shameel M. Studies on the bioactivity and elementology of marine algae from the coast of Karachi. Pak Phyt Res. 2004;18:865–72.CrossRefGoogle Scholar
  13. 13.
    Smit AJ. Medicinal and pharmaceutical uses of seaweed natural products: a review. J Appl Phycol. 2004;16:245–62.CrossRefGoogle Scholar
  14. 14.
    Del Val GA, Platas G, Basilio A. Screening of antimicrobial activities in red, green and brown macoalgae from Gran Canaria (Gran Canary Islands, Spain). Int Microbiol. 2001; 4: 35–40.Google Scholar
  15. 15.
    Alves PM, Leite PAAS, Pereira JV, Pereira LF, Pereira MSV, Higino JS, Lima EO. Antifungal activity of the extract of Psidium guajava Linn. (“goiabeira”) upon leavens of Candida of the oral cavity: an in vitro evaluation. Braz J Pharm. 2006; 16: 192–6Google Scholar
  16. 16.
    Vellinga A, Murphy AW, Hanahoe B, Bennett K, Cormican MA. A multilevel analysis of trimethoprim and ciprofloxacin prescribing and resistance of uropathogenic Escherichia coli in general practice. J Antimicrob Chemother. 2010;65:1514–20.PubMedCrossRefGoogle Scholar
  17. 17.
    Guimarães KG. Dihydroisocoumarin from Xyris pterygoblephara active against dermatophyte fungi. Phytochemistry. 2008;69:439–44.PubMedCrossRefGoogle Scholar
  18. 18.
    Sequeira BJ, Vital MJ, Pohlit AM, Pararols IC, Caúper GS. Antibacterial and antifungal activity of extracts and exudates of the Amazonian medicinal tree Himatanthus articulatus (Vahl) Woodson (common name: sucuba). Mem Inst Oswaldo Cruz. 2009;104:659–61.PubMedCrossRefGoogle Scholar
  19. 19.
    Ostrosky EA, Mizumoto MK, Lima MEL, Kaneko TM, Nishikawa SO, Freitas BR. Methods for evaluation of the antimicrobial activity and determination of minimum inhibitory concentration (MIC) of plant extracts. Rev Bras Farmacogn. 2008;18:301–7.CrossRefGoogle Scholar
  20. 20.
    Clinical and Laboratory Standard Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of filamentous fungi. Approved Standard M38-A, Wayne, PA. 2002.Google Scholar
  21. 21.
    Fernandez-Torres B, Cabanes FJ, Carrillo-Munoz AJ, Inza I, Guarro J. Collaborative evaluation of optimal antifungal susceptibility testing condition for dermatophytes. J Clin Microbiol. 2002; 40: 3999–4003.Google Scholar
  22. 22.
    Barros MES, Santos DA, Hamdan JS. Evaluation of susceptibility of Trichophyton mentagrophytes and Trichophyton rubrum clinical isolates to antifungal drugs using a modified CLSI microdilution method (M38-A). J Clin Microbiol. 2007; 56: 514–18.Google Scholar
  23. 23.
    Clinical and Laboratory Standard Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of yeast fungi. Approved Standard Document M27-A, Wayne PA. 2008.Google Scholar
  24. 24.
    Chiheb I, Riadi H, Martinez-Lopez J, Dominguez SJF, Gomez VJA, Bouziane H, Kadiri M. Screening of antibacterial activity in marine green and brown macroalgae from the coast of Morocco. Afr J Biotechnol. 2009;8:1258–62.Google Scholar
  25. 25.
    Hellio C, Bremer G, Pons AM, Le Gal Y, Bourgougnon N. Inhibition of the development of microorganisms (bacteria and fungi) by extracts of marine algae from Brittany, France. Appl Microbial Biotechnol. 2000;54:543–9.CrossRefGoogle Scholar
  26. 26.
    Ballesteros E, Martin D, Uriz MJ. Biological activity of extracts from some Mediterranean macrophytes. Bot Mar 1982; 35: 481–5.Google Scholar
  27. 27.
    Shanmughapriya S, Aseer M, Sugathan S, Kiran SJ, Seghal G, Kalimuthusamy N. Antimicrobial activity of seaweeds extracts against multiresistant pathogens. Ann Microbiol. 2008;58:535–41.CrossRefGoogle Scholar
  28. 28.
    Sekine H, Ohonuki N, Sadamasu K. The inhibitory effect of the crude extract from a seaweed of Dygenea simplex C. Agardh on the in vitro cytopathic activity of HIV-1 and it’s antigen production. Chem Pharm Bull. 1995;43:1580–4.PubMedCrossRefGoogle Scholar
  29. 29.
    Bhakuni DS, Rawat DS. Bioactive marine natural products. USA: Anamaya Publishers and Springer; 2005. p. 346.Google Scholar
  30. 30.
    Melo VMM, Medeiros DA, Rios FJB, Castelar LIM, Carvalho AFFU. Antifungal properties of proteins (agglutinins) from the red algae Hypnea musciformis (Wulfen) Lamouroux. Bot Mar 1997; 40: 281–84Google Scholar
  31. 31.
    Cordeiro RA, Gomes VM, Carvalho AFFUM, Maciel VM. Effect of Proteins from the Red Seaweed Hypnea musciformis(Wulfen) Lamouroux on the Growth of Human Pathogen Yeasts. Braz Arch Biol Technol 2005; 49: 915–21.Google Scholar
  32. 32.
    Tuney BH, Cadirci D, Ünal A, Sukatar A. Antimicrobial activities of the extracts of marine algae from the coast of Urla (Izmir, Turkey). Turk J Biol. 2006;20:171–5.Google Scholar
  33. 33.
    Salvador N, Garreta AG, Lavelli L, Ribera MA. Antimicrobial activity of Iberian macroalgae. Sci Mar. 2007;71:101–13.CrossRefGoogle Scholar
  34. 34.
    Orandy MA, Verde MJ, Martinez-Lozano SJ, Waksman NH. Active fractions from species of marine algae. Intern J Exp Bot 2004; 165–70.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Elica Amara Cecilia Guedes
    • 1
    Email author
  • Maria Anilda dos Santos Araújo
    • 2
  • Aryanna Kelly Pinheiro Souza
    • 2
  • Larissa Isabela Oliveira de Souza
    • 2
  • Lurdiana Dayse de Barros
    • 3
  • Fernanda Cristina de Albuquerque Maranhão
    • 4
  • Antônio Euzébio Goulart Sant’Ana
    • 3
  1. 1.Instituto de Química e Biotecnologia, Laboratório de Pesquisa em Recursos Naturais/IQB and Laboratório de Ficologia/ICBS Universidade Federal de AlagoasMaceióBrazil
  2. 2.Faculdade de Ciências Biológicas e da Saúde, Laboratório de MicologiaCentro Universitário CesmacMaceióBrazil
  3. 3.Instituto de Química e Biotecnologia, Laboratório de Pesquisa em Recursos Naturais/IQBUniversidade Federal de AlagoasMaceióBrazil
  4. 4.Instituto de Ciências Biológicas e da Saúde, Laboratório de Microbiologia Geral e ClínicaUniversidade Federal de AlagoasMaceióBrazil

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