Skip to main content

Advertisement

SpringerLink
Log in

Anticandidal Efficacy of Cinnamon Oil Against Planktonic and Biofilm Cultures of Candida parapsilosis and Candida orthopsilosis

  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Candida parapsilosis is yeast capable of forming biofilms on medical devices. Novel approaches for the prevention and eradication of the biofilms are desired. This study investigated the anticandidal activity of sixteen essential oils on planktonic and biofilm cultures of C. parapsilosis complex. We used molecular tools, enumeration of colony-forming units, the colourimetric MTT assay, scanning electron microscopy (SEM) and a chequerboard assay coupled with software analyses to evaluate the growth kinetics, architecture, inhibition and reduction in biofilms formed from environmental isolates of the Candida parapsilosis complex; further, we also evaluated whether essential oils would interact synergistically with amphotericin B to increase their anticandidal activities. Of the environmental C. parapsilosis isolates examined, C. parapsilosis and C. orthopsilosis were identified. Biofilm growth on polystyrene substrates peaked within 48 h, after which growth remained relatively stable up to 72 h, when it began to decline. Details of the architectural analysis assessed by SEM showed that C. parapsilosis complex formed less complex biofilms compared with C. albicans biofilms. The most active essential oil was cinnamon oil (CO), which showed anticandidal activity against C. orthopsilosis and C. parapsilosis in both suspension (minimum inhibitory concentration—MIC—250 and 500 μg/ml) and biofilm (minimum biofilm reduction concentration—MBRC—1,000 and 2,000 μg/ml) cultures. CO also inhibited biofilm formation (MBIC) at concentrations above 250 μg/ml for both species tested. However, synergism with amphotericin B was not observed. Thus, CO is a natural anticandidal agent that can be effectively utilised for the control of the yeasts tested.

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
Fig. 5

Similar content being viewed by others

References

  1. Pfaller MA, Messer SA, Boyken L, Tendolkar S, Hollis RJ, Diekema DJ. Geographic variation in the susceptibilities of invasive isolates of Candida glabrata to seven systemically active antifungal agents: a global assessment from the ARTEMIS Antifungal surveillance program conducted in 2001 and 2002. J Clin Microbiol. 2004;42:3142–6.

    Article  PubMed  CAS  Google Scholar 

  2. Mujica MT, Finquelievich JL, Jewtuchowicz V, Iovannitti CA. Prevalence of Candida albicans and Candida non-albicans in clinical samples during 1999–2001. Rev Argent Microbiol. 2004;36:107–12.

    PubMed  CAS  Google Scholar 

  3. Nucci M, Queiroz-Telles F, Tobón AM, Restrepo A, Colombo AL. Epidemiology of opportunistic fungal infections in Latin America. Clin Infect Dis. 2010;51:561–70.

    Article  PubMed  Google Scholar 

  4. Medrano DJ, Brilhante RS, Cordeiro A, Rocha MF, Rabenhorst SH, Sidrim JJ. Candidemia in a Brazilian hospital: the importance of Candida parapsilosis. Rev Inst Med Trop Sao Paulo. 2006;48:17–20.

    Article  PubMed  Google Scholar 

  5. Tavanti A, Davidson AD, Gow NAR, Maiden MCJ, Odds FC. Candida orthopsilosis and Candida metapsilosis spp nov. To replace Candida parapsilosis groups II and III. J Clin Microbiol. 2005;43:284–92.

    Article  PubMed  CAS  Google Scholar 

  6. Baillie GS, Douglas JL. Effect of growth rate on resistance of Candida albicans biofilms to antifungal agents. Antimicrob Agents Chemother. 1998;42:1900–5.

    PubMed  CAS  Google Scholar 

  7. Mah TC, O’Toole GA. Mechanism of biofilm resistance to anticandidal agents. Trends Microbiol. 2001;9:34–9.

    Article  PubMed  CAS  Google Scholar 

  8. Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother. 2002;46:1773–80.

    Article  PubMed  CAS  Google Scholar 

  9. Seneviratne CJ, Samaranayake LP. Biofilm lifestyle of Candida: a mini review. Oral Dis. 2008;14:582–90.

    Article  PubMed  CAS  Google Scholar 

  10. Cowan MM. Plant products as anticandidal agents. Clin Microbiol Rev. 1999;12:564–82.

    PubMed  CAS  Google Scholar 

  11. Oliveira DR, Leitão GG, Santos SS, Bizzo DHR, Lopes D, Alviano CS, Alviano DS, Leitão SG. Ethnopharmacological study of two Lippia species from Oriximina, Brazil. J Ethnopharmacol. 2006;108:103–8.

    Article  PubMed  CAS  Google Scholar 

  12. Mesa-Arango AC, Montiel-Ramos J, Zapata B, Duran C, Betancur-Galvis L, Stashenko E. Citral and carvone chemotypes from the essential oils of Colombian Lippia alba (Mill.) N.E. Brown: composition, cytotoxicity and antifungal activity. Mem Inst Oswaldo Cruz. 2009;104:878–84.

    Article  PubMed  CAS  Google Scholar 

  13. Giordani R, Regli P, Kaloustian J, Mikaïl C, Abou L, Portugal H. Antifungal effect of various essential oils against Candida albicans. Potentiation of antifungal action of amphotericin B by essential oil from Thymus vulgaris. Phytother Res. 2004;18:990–5.

    Article  PubMed  CAS  Google Scholar 

  14. Shelef LA. Anticandidal effects of spices. J Food Saf. 1983;6:29–44.

    Article  Google Scholar 

  15. Tavares AC, Gonçalves MJ, Cavaleiro C, Cruz MT, Lopes MC, Canhoto J, Salgueiro LR. Essential oil of Daucus carota subsp. halophilus: composition, antifungal activity and cytotoxicity. J Ethnopharmacol. 2008;119:129–34.

    Article  PubMed  CAS  Google Scholar 

  16. Nuryastuti T, van der Mei HC, Busscher HJ, Iravati S, Aman AT, Krom BP. Effect of cinnamon oil on icaA expression and biofilm formation by Staphylococcus epidermidis. Appl Environ Microbiol. 2009;75:6850–5.

    Article  PubMed  CAS  Google Scholar 

  17. Ali I, Khan FG, Suri KA, Gupta BD, Satti NK, Dutt P, Afrin F, Qazi GN, Khan IA. In vitro antifungal activity of hydroxychavicol isolated from Piper betle L. Ann Clin Microbiol Antimicrob. 2010;3:7–9.

    Article  Google Scholar 

  18. Knobloch K, Pauli A, Iberl B, Weigand H, Weis N. Antibacterial and antifungal properties of essential oils components. J Ess Oil Res. 1989;1:119–28.

    CAS  Google Scholar 

  19. Alviano WS, Mendonça-Filho RR, Alviano DS, Bizzo HR, Souto-Padrón T, Rodrigues ML, Bolognese AM, Alviano CS, Souza MM. Anticandidal activity of Croton cajucara Benth linalool-rich essential oil on artificial biofilms and planktonic microorganisms. Oral Microbiol Immunol. 2005;20:101–5.

    Article  PubMed  CAS  Google Scholar 

  20. Dalleau S, Cateau E, Bergès T, Berjeaud JM, Imbert C. In vitro activity of terpenes against Candida biofilms. Int J Antimicrob Agents. 2008;31:572–6.

    Article  PubMed  CAS  Google Scholar 

  21. Thaweboon S, Thaweboon B. In vitro anticandidal activity of Ocimum americanum L. essential oil against oral microorganisms. Southeast Asian J Trop Med Public Health. 2009;40:1025–33.

    PubMed  Google Scholar 

  22. Möller EM, Bahnweg G, Sandermann H, Geiger HH. A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Res. 1992;25:6115–6.

    Article  Google Scholar 

  23. National Committee for Clinical Laboratory Standards. Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard, 2nd ed. NCCLS document M27–A2. Wayne, PA: National Committee for Clinical Laboratory Standards; 2002.

    Google Scholar 

  24. Canton E, Peman J, Viudes A, Quindos G, Gobernado M, Espinel-Ingroff A. Minimum fungicidal concentrations of amphotericin B for bloodstream Candida species. Diagn Microbiol Infect Dis. 2003;45:203–6.

    Article  PubMed  CAS  Google Scholar 

  25. Ramage G, Saville SP, Wickes BL, Lopez-Ribot JL. Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol. 2004;68:5459–63.

    Article  Google Scholar 

  26. Krom BP, Cohen JB, Feser GEM, Cihlar RL. Optimized candidal biofilm microtiter assay. J Microbiol Methods. 2007;68:421–3.

    Article  PubMed  CAS  Google Scholar 

  27. Karpanen TJ, Worthington T, Hendry ER, Conway BR, Lambert PA. Anticandidal efficacy of chlorhexidine digluconate alone and in combination with eucalyptus oil, tea tree oil and thymol against planktonic and biofilm cultures of Staphylococcus epidermidis. J Antimicrob Chemother. 2008;62:1031–6.

    Article  PubMed  CAS  Google Scholar 

  28. Priester JH, Horst AM, Van de Werfhorst LC, Saleta JL, Mertes LA, Holden PA. Enhanced visualization of microbial biofilms by staining and environmental scanning electron microscopy. J Microbiol Methods. 2007;68:577–87.

    Article  PubMed  CAS  Google Scholar 

  29. Hendry ER, Worthington T, Conway BR, Lambert PA. Anticandidal efficacy of eucalyptus oil and 1,8-cineole alone and in combination with chlorhexidine digluconate against microorganisms grow in planktonic and biofilms cultures. J Antimicrob Chemother. 2009;64:1219–25.

    Article  PubMed  CAS  Google Scholar 

  30. 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.

    Article  PubMed  CAS  Google Scholar 

  31. Mastura M, Nor Azah MA, Khozirah S, Mawardi R, Manaf AA. Anticandidal and antidermatophic activity of Cinnamomum species oils. Cytobios. 1999;98:17–23.

    PubMed  CAS  Google Scholar 

  32. Mondello F, De Bernardis F, Girolamo A, Salvatore G, Cassone A. In vitro and in vivo activity of tea tree oil against azole-susceptible and -resistant human pathogenic yeasts. J Antimicrob Chemother. 2003;51:1223–9.

    Article  PubMed  CAS  Google Scholar 

  33. Romano L, Battaglia F, Masucci L, Sanguinetti M, Posteraro B, Plotti G, Zanetti S, Fadda G. In vitro activity of bergamot natural essence and furocoumarin-free and distilled extracts, and their associations with boric acid, against clinical yeast isolates. J Antimicrob Chemother. 2005;55:110–4.

    Article  PubMed  CAS  Google Scholar 

  34. Pozzatti P, Scheid LA, Spader TB, Atayde ML, Santurio JM, Alves SH. In vitro activity of essential oils extracted from plants used as spices against fluconazole-resistant and fluconazole-susceptible Candida spp. Can J Microbiol. 2008;54:950–6.

    Article  PubMed  CAS  Google Scholar 

  35. Silva CB, Guterres SS, Weisheimer V, Schapoval EE. Antifungal activity of the lemongrass oil and citral against Candida spp. Braz J Infect Dis. 2008;12:63–6.

    Google Scholar 

  36. Lockhart SR, Messer SA, Tendolkar S, Diekema DJ. Geographic distribution and antifungal susceptibility of newly described species Candida orthopsilosis, in comparison to the closely-related species Candida parapsilosis. J Clin Microbiol. 2008;46:2659–64.

    Article  PubMed  CAS  Google Scholar 

  37. Gomez-Lopez A, Alastruey-Izquierdo A, Rodriguez D, Almilrante B, Pahissa A, Rodriguez-Tudela JL, Cuenca-Estrella M. Barcelona Candidemia Project Study Group. Prevalence and susceptibility profile of Candida metapsilosis and Candida orthopsilosis: results from population-based surveillance of candidemia in Spain. Antimicrob Agents Chemother. 2008;52:1506–9.

    Article  PubMed  CAS  Google Scholar 

  38. Silva AP, Miranda IM, Lisboa C, Pina-Vaz C, Rodrigues AG. Prevalence, distribution, and antifungal susceptibility profiles of Candida parapsilosis, C. orthopsilosis, and C. metapsilosis in a tertiary care hospital. J Clin Microbiol. 2009;47:2392–7.

    Article  PubMed  CAS  Google Scholar 

  39. Gonçalves SS, Amorim CS, Nucci M, Padovan AC, Briones MR, Melo AS, Colombo AL. Prevalence rates and antifungal susceptibility profiles of the Candida parapsilosis species complex: results from a nationwide surveillance of candidaemia in Brazil. Clin Microbiol Infect. 2010;16:885–7.

    PubMed  Google Scholar 

  40. Tay ST, Na SL, Chong J. Molecular differentiation and antifungal susceptibilities of Candida parapsilosis isolated from patients with bloodstream infections. J Med Microbiol. 2009;58:185–91.

    Article  PubMed  CAS  Google Scholar 

  41. Lattif AA, Mukherjee PK, Chandra J, Swindell K, Lockhart SR, Diekema DJ, Pfaller MA, Ghannoum MA. Characterization of biofilms formed by Candida parapsilosis, C. metapsilosis, and C. orthopsilosis. Int J Med Microbiol. 2010;300:265–70.

    Article  PubMed  Google Scholar 

  42. Melo AS, Bizerra FC, Freymüller E, Arthington-Skaggs BA, Colombo AL. Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med Mycol. 2011;49:253–62.

    Article  PubMed  CAS  Google Scholar 

  43. Nikawa H, Nishimura H, Hamada T, Makihira S, Samaranayake LP. Relationship between thigmotropism and Candida biofilm formation in vitro. Mycopathologia. 1998;144:125–9.

    Article  PubMed  Google Scholar 

  44. Seidler M, Salvenmoser S, Muller FM. In vitro effects of micafungin against Candida biofilms on polystyrene and central venous catheter sections. Int J Antimicrob Agents. 2006;28:568–73.

    Article  PubMed  CAS  Google Scholar 

  45. Thein ZM, Samaranayake YH, Samaranayake LP. In vitro biofilm formation of Candida albicans and non-albicans Candida species under dynamic and anaerobic conditions. Arch Oral Biol. 2007;52:761–7.

    Article  PubMed  CAS  Google Scholar 

  46. Andrews RE, Parks LW, Spence KD. Some effects of Douglas fir terpenes on certain microorganisms. Appl Environ Microbiol. 1980;40:301–4.

    PubMed  CAS  Google Scholar 

  47. Mercier B, Prost J, Prost M. The essential oil of turpentine and its major volatile fraction α- and β-pinenes: a review. Int J Occup Med Environ Health. 2009;22:331–42.

    Article  PubMed  Google Scholar 

  48. Shan B, Cai YZ, Brooks JD, Corke H. Antibacterial properties and major bioactive components of cinnamon stick (Cinnamon burmannii): activity against foodborne pathogenic bacteria. J Agric Food Chem. 2007;55:5484–90.

    Article  PubMed  CAS  Google Scholar 

  49. Prabuseenivasan S, Jayakumar M, Ignacimuthu S. In vitro antibacterial activity of some plant essential oils. BMC Complement Altern Med. 2006;6:39.

    Article  PubMed  Google Scholar 

  50. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15:167–93.

    Article  PubMed  CAS  Google Scholar 

  51. Farag RS, Daw ZY, Hewedi FM, Elbatory GSA. Anticandidal activity of some Egyptian spice essential oils. J Food Prot. 1989;52:665–7.

    CAS  Google Scholar 

  52. Nychas GJE. Natural anticandidals from plants. In: Gould GW, editor. New methods of food preservations. London, UK: Blackie Academic; 1995. p. 58–89.

    Chapter  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from Funded by Scientific Development Support Program of the School of Pharmaceutical Sciences at Unesp (PADC/FCFAr-UNESP proc. 2009/54) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). We thank Prof. Arnaldo Lopes Colombo for C. albicans SC5314, C. parapsilosis ATCC 90018, C. orthopsilosis ATCC 96141 and C. metapsilosis ATCC 96143 strains.

Author information

Authors and Affiliations

  1. Departamento de Análises Clínicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista (UNESP), Araraquara, SP, Brazil

    Regina Helena Pires, Ana Marisa Fusco Almeida, Marcelo T. Matsumoto & Maria José S. Mendes-Giannini

  2. Laboratório de Pesquisa em Microbiologia Aplicada, Universidade de Franca (UNIFRAN), Franca, SP, Brazil

    Lilian Bueno Montanari, Carlos Henrique G. Martins & José Eduardo Zaia

  3. Rua Expedicionários do Brasil, 1621, Araraquara, SP, 14801-902, Brazil

    Maria José S. Mendes-Giannini

Authors
  1. Regina Helena Pires
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lilian Bueno Montanari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carlos Henrique G. Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José Eduardo Zaia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ana Marisa Fusco Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marcelo T. Matsumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Maria José S. Mendes-Giannini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria José S. Mendes-Giannini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pires, R.H., Montanari, L.B., Martins, C.H.G. et al. Anticandidal Efficacy of Cinnamon Oil Against Planktonic and Biofilm Cultures of Candida parapsilosis and Candida orthopsilosis . Mycopathologia 172, 453–464 (2011). https://doi.org/10.1007/s11046-011-9448-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-011-9448-0

Keywords

Search

Navigation