Skip to main content

Advertisement

SpringerLink
Log in

Essential Oils, Silver Nanoparticles and Propolis as Alternative Agents Against Fluconazole Resistant Candida albicans, Candida glabrata and Candida krusei Clinical Isolates

  • Original Article
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Development of effective and safe therapeutic treatment of fungal infections remains one of the major challenge for modern medicine. The aim of presented investigation was to analyze the in vitro antifungal activity of selected essential oils, ethanolic extracts of propolis and silver nanoparticles dropped on TiO2 against azole-resistant C. albicans (n = 20), C. glabrata (n = 14) and C. krusei (n = 10) clinical isolates. Among tested essential oils, the highest activity has definitely been found in the case of the oil isolated from the bark of Cinnamomum cassia, with MIC and MFC values for all tested strains in the range of 0.0006–0.0097 % (v/v) and 0.0012–0.019 % (v/v), respectively. High activity was also observed for the Lemon, Basil, Thyme, Geranium and Clove (from buds) essential oils. Significant differences in fungicidal activity have been observed in the case of four tested propolis samples. Only one of them revealed high activity, with MFC values in the range from 0.156 to 1.25 % (v/v). Satisfactory fungicidal activity, against C. albicans and C. glabrata isolates, was also observed in the case of silver nanoparticles, however C. krusei isolates were mostly resistant. We also revealed that constituents of most of essential oils and propolis as well as silver nanoparticles are not substrates for drug transporters, which belong to the most important factors affecting resistance of Candida spp. clinical isolates to many of conventional antimycotics. To conclude, the results of our investigation revealed that essential oils, propolis and silver nanoparticles represent high potential for controlling and prevention candidiasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Calderone RA (2002) Introduction and historical perspectives. Candida and Candidiasis. ASM Press, Washington, DC, pp 15–25

    Google Scholar 

  2. Pfaller MA, Diekema DJ (2004) Rare and emerging opportunistic fungal pathogens: concern for resistance beyond Candida albicans and Aspergillus fumigatus. J Clin Microbiol 42:4419–4431. doi:10.1128/JCM.42.10.4419-4431.2004

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J (2012) Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev 36:288–305. doi:10.1111/j.1574-6976.2011.00278.x

    Article  CAS  PubMed  Google Scholar 

  4. Low Ch-Y, Rotstein C (2011) Emerging fungal infections in immunocompromised patients. Med Rep 3:14

    Google Scholar 

  5. Pfaller MA, Diekema DJ (2010) Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 36:1–53. doi:10.3109/10408410903241444

    Article  PubMed  Google Scholar 

  6. Pfaller MA, Diekema DJ (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133–163. doi:10.1128/CMR.00029-06

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Papon N, Courdavault V, Clastre M, Bennett RJ (2013) Emerging and emerged pathogenic Candida species: beyond the Candida albicans paradigm. PLoS Pathog 9:e1003550. doi:10.1371/journal.ppat.1003550

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Edlind TD, Katiyar SK (2010) Mutational analysis of flucytosine resistance in Candida glabrata. Antimicrob Agents Chemother 54:4733–4738. doi:10.1128/AAC.00605-10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Romanowska E (2008) Mechanizmy oporności grzybów na leki przeciwgrzybicze/Fungal resistance mechanisms on antifungal agents. In: Dzierżanowska D (ed) Zakażenia szpitalne. α – medica press, Bielsko-Biała, pp 497–507 (in Polish)

  10. Vermes A, Guchelaar HJ, Dankert J (2000) Flucytosine: a review of its pharmacology, clinical indications, pharmacokinetics, toxicity and drug interactions. J Antimicrob Chemother 46:171–179. doi:10.1093/jac/46.2.171

    Article  CAS  PubMed  Google Scholar 

  11. Kurek A, Grudniak AM, Kraczkiewicz-Dowjat A, Wolska KI (2011) New antibacterial therapeutics and strategies. Pol J Microbiol 60:3–12

    CAS  PubMed  Google Scholar 

  12. Rajeshkumar R, Sundararman M (2012) Emergence of Candida spp. and exploration of natural bioactive molecules for anticandidal therapy—status quo. Mycoses 55:e60–e73. doi:10.1111/j.1439-0507.2011.02156.x

    Article  PubMed  Google Scholar 

  13. Franz R, Ruhnke M, Morschhaüser J (1999) Molecular aspects of fluconazole resistance development in Candida albicans. Mycoses 42:453–458. doi:10.1046/j.1439-0507.1999.00498.x

    Article  CAS  PubMed  Google Scholar 

  14. Zielinska A, Kowalska E, Sobczak JW, Lacka I, Gazda M, Ohtani B, Hupka J, Zaleska A (2010) Silver-doped TiO2 prepared by microemulsion method; surface properties, bio- and photoactivity. Sep Purif Tech 72:309–318. doi:10.1016/j.seppur.2010.03.002

    Article  CAS  Google Scholar 

  15. Clinical Laboratory Standards Institute (CLSI) (2008) Reference method for broth dilution antifungal susceptibility testing of yeasts: third edition (M27-A3). CLSI, Wayne

    Google Scholar 

  16. de Castro PA, Bom VL, Brown NA, de Almeida RS, Ramalho LN, Savoldi M, Goldman MH, Berretta AA, Goldman GH (2013) Identification of the cell targets important for propolis-induced cell death in Candida albicans. Fungal Genet Biol 60:74–86. doi:10.1016/j.fgb.2013.07.001

    Article  PubMed  Google Scholar 

  17. Romanowska E (2010) Zakażenia grzybicze/Fungal infections. In: Piegdoń (ed) Pielęgniarstwo epidemiologiczne. Instytut Pomnik Centrum Zdrowia Dziecka, Warszawa, pp 58–65 (in Polish)

  18. Panacek A, Kolar M, Vecerova R, Prucek R, Soukupova J, Krystof V, Hamal P, Zboril R, Kvitek L (2009) Antifungal activity of silver nanoparticles against Candida spp. Biomaterials 30:6333–6340. doi:10.1016/j.biomaterials.2009.07.065

    Article  CAS  PubMed  Google Scholar 

  19. Kim KS, Kim YS, Han I, Kim M-H, Jung MH, Park H-K (2011) Quantitative and qualitative analyses of the cell death process in Candida albicans treated by antifungal agents. PLoS One 6:e28176. doi:10.1371/journal.pone.0028176

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Carvalhinho S, Costa AM, Coelho AC, Martins E, Sampaio A (2012) Susceptibilities of Candida albicans mouth isolates to antifungal agents. Essential oils and mouth rinses. Mycophatologia 174:69–76. doi:10.1007/s11046-012-9520-4

    Article  CAS  Google Scholar 

  21. Bialon M, Krzysko-Lupicka T, Koszalkowska M, Wieczorek PP (2014) The influence of chemical composition of commercial lemon essential oils on the growth of Candida strains. Mycopathologia 17:29–39. doi:10.1007/s11046-013-9723-3

    Article  Google Scholar 

  22. Pozzatti P, Scheid LA, Spader TB, Atayde ML, Santurio JM, Alves SH (2008) In vitro activity of essential oils extracted from plants used as spices against fluconazole-resistant and fluconazole-susceptible Candida spp. Can J Microbiol 54:950–956. doi:10.1139/w08-097

    Article  CAS  PubMed  Google Scholar 

  23. Pozzatti P, Loreto ES, Lopes PG, Athayde ML, Santurio JM, Alves SH (2010) Comparison of the susceptibilities of clinical isolates of Candida albicans and Candida dubliniensis to essential oils. Mycoses 53:12–15. doi:10.1111/j.1439-0507.2008.01643.x

    Article  CAS  PubMed  Google Scholar 

  24. Budzynska A, Sadowska B, Lipowczan G, Maciag A, Kalemba D, Rozalska B (2013) Activity of selected essential oils against Candida spp. trains. Evaluation of new aspects of their specific pharmacological properties, with special reference to Lemon balm. Adv Microbiol 3:317–325. doi:10.4236/aim.2013.34045

    Article  Google Scholar 

  25. Ooi LS, Li Y, Kam SL, Wang H, Wong EY, Ooi VE (2006) Antimicrobial activities of cinnamon oil and cinnamaldehyde from the Chinese medicinal herb Cinnamomum cassia Blume. Am J Chin Med 34:511–522. doi:10.1142/S0192415X06004041

    Article  CAS  PubMed  Google Scholar 

  26. Dota KF, Consolaro ME, Svidzinski TI, Bruschi ML (2011) Antifungal activity of Brazilian propolis microparticles against yeasts isolated from vulvovaginal candidiasis. Evid Based Complement Alternat Med. 2011:201953. doi:10.1093/ecam/neq029

    Article  PubMed Central  PubMed  Google Scholar 

  27. Shokri H, Khosravi AR, Yalfani R (2011) Antifungal efficacy of propolis against fluconazole-resistant Candida glabrata isolates obtained from women with recurrent vulvovaginal candidiasis. Int J Gynaecol Obstet 114:158–159. doi:10.1016/j.ijgo.2011.02.019

    Article  PubMed  Google Scholar 

  28. Astani A, Zimmermann S, Hassan E, Reichling J, Sensch KH, Schnitzler P (2013) Antimicrobial activity of propolis special extract GH 2002 against multidrug-resistant clinical isolates. Pharmazie 68:695–701

    CAS  PubMed  Google Scholar 

  29. Capistrano HM, de Assis EM, Leal RM, Alvrez-Leite ME, Brener S, Bastos EM (2013) Brazilian green propolis compared to miconazole gel in the treatment of Candida-associated denture stomatitis. Evid Based Complement Alternat Med 2013:947980. doi:10.1155/2013/947980

    Article  PubMed Central  PubMed  Google Scholar 

  30. Isla MI, Dantur Y, Salas A, Danert C, Zampini C, Arias M, Ordonez R, Maldonado L, Bedascarrasbure E, Nieva Moreno MI (2012) Effect of seasonality on chemical composition and antibacterial and anticandida activities of Argentine propolis. Design of a topical formulation. Nat Prod Commun 7:1315–1318

    CAS  PubMed  Google Scholar 

  31. Falcao SI, Vale N, Cos P, Gomes P, Freire C, Maes L, Vilas-Boas M (2014) In vitro evaluation of portuguese propolis and floral sources for antiprotozoal, antibacterial and antifungal activity. Phytother Res 28:437–443. doi:10.1002/ptr.5013

    Article  PubMed  Google Scholar 

  32. Monzote L, Cuesta-Rubio O, Campo Fernandez M, Marquez Hernandez I, Fraga J, Perez K, Kerstens M, Maes L, Cos P (2012) In vitro antimicrobial assessment of Cuban propolis extracts. Mem Inst Oswaldo Cruz 107:978–984. doi:10.1590/S0074-02762012000800003

    Article  PubMed  Google Scholar 

  33. Kim KJ, Sung WS, Suh BK, Moon SK, Choi JS, Kim JG, Lee DG (2009) Antifungal activity and mode of action of silver nano-particles on Candida albicans. Biometals 22:235–242. doi:10.1007/s10534-008-9159-2

    Article  CAS  PubMed  Google Scholar 

  34. Jebali A, Hajjar FH, Pourdanesh F, Hekamtimoghaddam S, Kazemi B, Masoudi A, Daliri K, Sedighi N (2014) Silver and gold nanostructures: antifungal property of different shapes of these nanostructures on Candida species. Med Mycol 52:65–72. doi:10.3109/13693786.2013.822996

    PubMed  Google Scholar 

  35. Gupta K, Barua S, Hazarika NS, Manhar AK, Nath D, Karak N, Namsa ND, Mukhopadhyay R, Kalia VC, Mandal M (2014) Green silver nanoparticles: enhanced antimicrobial and antibiofilm activity with effects on DNA replication and cell cytotoxicity. RSC Adv 4:52845–52855. doi:10.1039/C4RA08791G

    Article  CAS  Google Scholar 

  36. Zaleska A (2008) Doped TiO2; a review. Recent Patents Eng 2:157–164. doi:10.2174/187221208786306289

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the grant no N N405 151040 from the National Science Centre in Poland. The authors are also grateful to Teresa Tanczyk, from Pollena-Aroma and Marta Schielmann from Gdansk University of Technology, for their help in preparing the manuscript.

Conflict of interest

Authors do not declare any conflict of interest.

Author information

Authors and Affiliations

  1. Department of Pharmaceutical Technology and Biochemistry, Faculty of Chemistry, Gdansk University of Technology, ul. G. Narutowicza 11/12, 80-233, Gdansk, Poland

    Piotr Szweda, Katarzyna Gucwa & Sławomir Milewski

  2. Department of Clinical Microbiology and Immunology, The Children’s Memorial Health Institute, Aleja Dzieci Polskich 20, 04-730, Warsaw, Poland

    Ewa Romanowska & Katarzyna Dzierżanowska-Fangrat

  3. Department of Chemical Technology, Faculty of Chemistry, Gdansk University of Technology, ul. G. Narutowicza 11/12, 80-233, Gdansk, Poland

    Anna Zielińska Jurek

  4. Department of Pharmacognosy, Wroclaw Medical University, ul. Borowska 211a, 50-556, Wroclaw, Poland

    Piotr Marek Kuś

  5. Department of Molecular Biotechnology and Microbiology, Faculty of Chemistry, Gdansk University of Technology, ul. G. Narutowicza 11/12, 80-233, Gdansk, Poland

    Ewelina Kurzyk

Authors
  1. Piotr Szweda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katarzyna Gucwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ewelina Kurzyk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ewa Romanowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katarzyna Dzierżanowska-Fangrat
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anna Zielińska Jurek
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Piotr Marek Kuś
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sławomir Milewski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Piotr Szweda.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Szweda, P., Gucwa, K., Kurzyk, E. et al. Essential Oils, Silver Nanoparticles and Propolis as Alternative Agents Against Fluconazole Resistant Candida albicans, Candida glabrata and Candida krusei Clinical Isolates. Indian J Microbiol 55, 175–183 (2015). https://doi.org/10.1007/s12088-014-0508-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12088-014-0508-2

Keywords

Search

Navigation