Advertisement

Electrospun essential oil-polycaprolactone nanofibers as antibiofilm surfaces against clinical Candida tropicalis isolates

  • Gulcan SahalEmail author
  • Behzad Nasseri
  • Aliakbar Ebrahimi
  • Isil Seyis Bilkay
Original Research Paper

Abstract

Objective

As an approach to prevent biofilm infections caused by Candida tropicalis on various surfaces, determination of effect of biodegradable polycaprolactone nanofibers (PCLNFs) with different concentrations of two different essential oils were tested in this study.

Results

Both of the tested essential oils exhibited antifungal effect (minimal inhibitory concentration; 0.25–0.49 µL/mL, minimal fungicidal concentration; 0.25–0.49 µL/mL, depending on the C. tropicalis strain) (Zone of inhibition caused by 500 μL/mL concentration of oils; 28–56 mm). 0, 2, 4% clove oil PCLNFs and 0, 2, 4% red thyme oil-PCLNFs were free from bead formation and uniform in diameter. Diameters of all essential oil containing PCLNFs were ranged from 760 to 1100 nm and were significantly different from 0% essential oil-PCLNF (P < 0.05). 0, 2, 4% clove oil-PCLNFs were significantly more hydrophobic compared to 8% clove oil-PCLNF (P < 0.01), whereas 0% and 2% red thyme oil-PCLNFs were significantly more hydrophobic compared to 4% and 8% red thyme oil PCLNFs (P < 0.01). Highest amount of biofilm inhibition was observed by 4% clove oil-PCLNF and by 4% red thyme oil-PCLNF.

Conclusions

Clove and red thyme oils may be used not only as antifungals but also as biofilm inhibitive agents on surfaces of biomaterials that are frequently contaminated by C. tropicalis, when they are incorporated into PCLNFs.

Keywords

Antibiofilm Candida tropicalis Electrospun biodegradable nanofibers Essential oils Polycaprolactone 

Notes

Acknowledgements

We are grateful to Scientific Research Projects Coordination Unit of Hacettepe University, Ankara, Turkey for supporting this study (Grant No.: FHD-2017-13075) and also to the Scientific and Technological Research Council of Turkey, 1003 project (TUBITAK project No: 113O864) for the production of nanofibers.

Funding

This study was supported by the funding received from Scientific Research Projects Coordination Unit (grant number: FHD-2017-13075) of Hacettepe University, Ankara, Turkey. Additionally, production of nanofibers was supported by the Scientific and Technological Research Council of Turkey, 1003 project (TUBITAK project No: 113O864) and Behzad Nasseri and Aliakbar Ebrahimi were also supported by the mentioned project.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ahire JJ, Hattingh M, Neveling DP, Dicks LMT (2016) Copper-containing anti-biofilm nanofiber scaffolds as a wound dressing material. PLoS ONE 11(3):e0152755CrossRefGoogle Scholar
  2. Akthar MS, Degaga B, Azam T (2014) Antimicrobial activity of essential oils extracted from medicinal plants against the pathogenic microorganisms: a review. Biol Sci Pharm Res 2(1):001–007Google Scholar
  3. Alharbi HF, Luqman M, Khan ST (2018) Antibiofilm activity of synthesized electrospun core-shell nanofiber composites of PLA and PVA with silver nanoparticles. Mater Res Express.  https://doi.org/10.1088/2053-1591/aad4df Google Scholar
  4. Alshaikh N, Perveen K (2017) Anti-candidal activity and chemical composition of essential oil of clove (Syzygium aromaticum). J Essent Oil Bear Plants 20(4):951–958CrossRefGoogle Scholar
  5. Asghari F, Samiei M, Adibkia K, Akbarzadeh A, Davaran S (2017) Biodegradable and biocompatible polymers for tissue engineering application: a review. Artif Cells Nanomed Biotechnol 45(2):185–192CrossRefGoogle Scholar
  6. Ashbaugh AG, Jiang X, Zheng J, Tsai AS et al (2016) Polymeric nanofiber coating with tunable combinatorial antibiotic delivery prevents biofilm-associated infection in vivo. Proc Natl Acad Sci USA 113:E6919–E6928CrossRefGoogle Scholar
  7. Ballester-Costa C, Sendra E, Fernández-López J, Pérez-Álvarez JA, Viuda-Martos M (2017) Assessment of antioxidant and antibacterial properties on meat homogenates of essential oils obtained from four thymus species achieved from organic growth. Foods 6(8):59CrossRefGoogle Scholar
  8. Campoccia D, Montanaro L, Arciola CR (2013) A review of the clinical implications of anti-infective biomaterials and infection-resistant surfaces. Biomaterials 34(33):8018–8029CrossRefGoogle Scholar
  9. Chen M, Yu Q, Sun H (2013) Novel strategies for the prevention and treatment of biofilm related infections. Int J Mol Sci 14(9):18488–18501CrossRefGoogle Scholar
  10. Coad BR, Kidd SE, Ellis DH, Griesser HJ (2014) Biomaterials surfaces capable of resisting fungal attachment and biofilm formation. Biotechnol Adv 32(2):296–307CrossRefGoogle Scholar
  11. de Oliveira Mori CLS, dos Passos NA, Oliveira JE, Mattoso LHC, Mori FA, Carvalho AG, de Souza Fonseca A, Tonoli GHD (2014) Electrospinning of zein/tannin bio-nanofibers. Ind Crops Prod 52:298–304CrossRefGoogle Scholar
  12. de Paula SB, Bartelli TF, Di Raimo V, Santos JP, Morey AT, Bosini MA, Nakamura CV, Yamauchi LM, Yamada-Ogatta SF (2014) Effect of eugenol on cell surface hydrophobicity, adhesion, and biofilm of Candida tropicalis and Candida dubliniensis isolated from oral cavity of HIV-infected patients. Evid Based Complement Alternat Med 2014:505204CrossRefGoogle Scholar
  13. Di Lorenzo A, Bloise N, Meneghini S, Sureda A, Tenore GC, Visai L, Arciola CR, Daglia M (2016) Effect of winemaking on the composition of red wine as a source of polyphenols for anti-infective biomaterials. Materials (Basel) 9(5):316CrossRefGoogle Scholar
  14. Dong ZX, Wu YQ, Wang Q, Xie C, Ren YF, Clark RL (2012) Reinforcement of electrospun membranes using nanoscale Al2O3 whiskers for improved tissue scaffolds. J Biomed Mater Res A 100(4):903–910CrossRefGoogle Scholar
  15. Hirasawa M, Tsutsumi-Arai C, Takakusaki K, Oya T, Fueki K, Wakabayashi N (2018) Superhydrophilic co-polymer coatings on denture surfaces reduce Candida albicans adhesion-An in vitro study. Arch Oral Biol 27(87):143–150CrossRefGoogle Scholar
  16. Hong JK, Madihally SV (2010) Three-dimensional scaffold of electrosprayed fibers with large pore size for tissue regeneration. Acta Biomater 6(12):4734–4742CrossRefGoogle Scholar
  17. Hu X, Liu S, Zhou G, Huang Y, Xie Z, Jing X (2014) Electrospinning of polymeric nanofibers for drug delivery applications. J Control Release 185:12–21CrossRefGoogle Scholar
  18. Karami Z, Rezaeian I, Zahedi P, Abdollahi M (2013) Preparation and performance evaluations of electrospun poly(ε-caprolactone), poly(lactic acid), and their hybrid (50/50) nanofibrous mats containing thymol as an herbal drug for effective wound healing. J Appl Polym Sci 129(2):756–766CrossRefGoogle Scholar
  19. Karuppuswamy P, Reddy Venugopal J, Navaneethan B, Luwang Laiva A, Ramakrishna S (2015) Polycaprolactone nanofibers for the controlled release of tetracycline hydrochloride. Mater Lett 141:180–186CrossRefGoogle Scholar
  20. Leal F, Taghouti M, Nunes F, Silva A, Coelho AC, Matos M (2017) Thymus plants: a review—micropropagation, molecular and antifungal activity, active ingredients from aromatic and medicinal plants. InTech. https://www.intechopen.com/books/active-ingredients-from-aromatic-and-medicinal-plants/thymus-plants-a-review-micropropagation-molecular-and-antifungal-activity. Accessed 03 January 2018
  21. Mountziaris PM, Tzouanas SN, Mikos AG (2010) Dose effect of tumor necrosis factor-α on in vitro osteogenic differentiation of mesenchymal stem cells on biodegradable polymeric microfiber scaffolds. Biomaterials 31(7):1666–1675CrossRefGoogle Scholar
  22. Negri M, Silva S, Henriques M, Azeredo J, Svidzinski T, Oliveira R (2011) Candida tropicalis biofilms: artificial urine, urinary catheters and flow model. Med Mycol 49(7):739–747Google Scholar
  23. Negri M, Silva S, Capoci IR, Azeredo J, Henriques M (2016) Candida tropicalis Biofilms: biomass, metabolic activity and secreted aspartyl proteinase production. Mycopathologia 181(3–4):217–224CrossRefGoogle Scholar
  24. Nguyen TH, Lee BT (2012) The effect of cross-linking on the microstructure, mechanical properties and biocompatibility of electrospun polycaprolactone–gelatin/plga–gelatin/plga–chitosan hybrid composite, science and technology of advanced materials. Sci Technol Adv Mater 13(3):035002CrossRefGoogle Scholar
  25. Omran SM, Esmailzadeh S (2009) Comparison of anti-candida activity of thyme, pennyroyal, and lemon essential oils versus antifungal drugs against Candida species. Jundishapur J Microbiol 2(2):53–60Google Scholar
  26. O’Toole GA (2011) Microtiter dish biofilm formation assay. J Vis Exp 47:2437Google Scholar
  27. Padalia H, Moteriya P, Baravalia Y, Chanda S (2015) Antimicrobial and synergistic effects of some essential oils to fight against microbial pathogens: a review. In: Méndez-Vilas A (ed) The battle against microbial pathogens: basic science, technological advances and educational programs. Formatex Microbiology Series, Badajoz, pp 34–45Google Scholar
  28. Panwar R, Pemmaraju SC, Sharma AK, Pruthi V (2016) Efficacy of ferulic acid encapsulated chitosan nanoparticles against Candida albicans biofilm. Microb Pathog 95:21–31CrossRefGoogle Scholar
  29. Phillips KS, Patwardhan D, Jayan G (2015) Biofilms, medical devices, and antibiofilm technology: key messages from a recent public workshop. Am J Infect Control 43(1):2–3CrossRefGoogle Scholar
  30. Pina-Vaz C, Gonçalves Rodrigues A, Pinto E, Costa-de-Oliveira S, Tavares C, Salgueiro L, Cavaleiro C, Gonçalves MJ, Martinez-de-Oliveira J (2004) Antifungal activity of thymus oils and their major compounds. J Eur Acad Dermatol Venereol 18(1):73–78CrossRefGoogle Scholar
  31. Pinto E, Vale-Silva L, Cavaleiro C, Salgueiro L (2009) Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J Med Microbiol 58(Pt 11):1454–1462CrossRefGoogle Scholar
  32. Potrč T, Baumgartner S, Roškar R, Planinšek O, Lavrič Z, Kristl J, Kocbek P (2015) Electrospun polycaprolactone nanofibers as a potential oromucosal delivery system for poorly water-soluble drugs. Eur J Pharm Sci 75:101–113CrossRefGoogle Scholar
  33. Puškárová A, Bučková M, Kraková L, Pangallo D, Kozics K (2017) The antibacterial and antifungal activity of six essential oils and their cyto/genotoxicity to human HEL 12469 cells. Sci Rep 7(1):8211CrossRefGoogle Scholar
  34. Radwan IA, Abed AH, Abeer MR, Ibrahim RA, Abdallah AS (2014) Effect of thyme, clove and cinnamon essential oils on Candida albicans and moulds isolated from different sources. Am J Anim Vet Sci 9(4):303–314CrossRefGoogle Scholar
  35. Rajkowska K, Otlewska A, Kunicka-Styczyńska A, Krajewska A (2017) Candida albicans impairments induced by peppermint and clove oils at sub-inhibitory concentrations. Int J Mol Sci 18(6):1307CrossRefGoogle Scholar
  36. Ramage G, Martínez JP, López-Ribot JL (2006) Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 6(7):979–986CrossRefGoogle Scholar
  37. Ramage G, Rajendran R, Sherry L, Williams C (2012) Fungal biofilm resistance. Int J Microbiol 2012:528521CrossRefGoogle Scholar
  38. Rodrigues V, Cabral C, Évora L, Ferreira I, Cavaleiro C, Cruz MT, Lígia S (2015) Chemical composition, anti-inflammatory activity and cytotoxicity of Thymus zygis L. subsp. sylvestris (Hoffmanns. & Link) Cout. essential oil and its main compounds. Arab J Chem.  https://doi.org/10.1016/j.arabjc.2015.08.026 Google Scholar
  39. Sadekuzzaman M, Yang S, Mizan MFR, Ha SD (2015) Current and recent advanced strategies for combating biofilms. Compr Rev Food Sci Food Saf 14(4):491–509CrossRefGoogle Scholar
  40. Sahal G, Bilkay IS (2018) Distribution of clinical isolates of Candida spp. and antifungal susceptibility of high biofilm forming Candida isolates. Rev Soc Bras Med Trop 51(5):644–650CrossRefGoogle Scholar
  41. Sakkas H, Papadopoulou C (2017) Antimicrobial activity of Basil, oregano, and thyme essential oils. J Microbiol Biotechnol 27(3):429–438CrossRefGoogle Scholar
  42. 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(2):288–305CrossRefGoogle Scholar
  43. Souza CM, Pereira Junior SA, Moraes Tda S, Damasceno JL et al (2016) Antifungal activity of plant-derived essential oils on Candida tropicalis planktonic and biofilms cells. Med Mycol 54(5):515–523CrossRefGoogle Scholar
  44. Velluti A, Sanchis V, Ramos AJ, Egido J, Marín S (2003) Inhibitory effect of cinnamon, clove, lemongrass, oregano and palmarose essential oils on growth and fumonisin B1 production by Fusarium proliferatum in maize grain. Int J Food Microbiol 89(2–3):145–154CrossRefGoogle Scholar
  45. von Eiff C, Jansen B, Kohnen W, Becker K (2005) Infections associated with medical devices: pathogenesis, management and prophylaxis. Drugs 65(2):179–214CrossRefGoogle Scholar
  46. Yadav R, Balasubramanian K (2015) Polyacrylonitrile/Syzygium aromaticum hierarchical hydrophilic nanocomposite as a carrier for antibacterial drug delivery systems. RSC Adv 5(5):3291–3298CrossRefGoogle Scholar
  47. Yoshimoto H, Shin YM, Terai H, Vacanti JP (2003) A biodegradable nanofiber scaffold by electrospinning BND its potential for bone tissue engineering. Biomaterials 24(12):2077–2082CrossRefGoogle Scholar
  48. Zander NE, Orlicki JA, Rawlett AM, Beebe TP (2012) Quantification of protein incorporated into electrospun polycaprolactone tissue engineering scaffolds. ACS Appl Mater Interfaces 4(4):2074–2081CrossRefGoogle Scholar
  49. Zapata PA, Larrea M, Tamayo L, Rabagliati FM, Azócar MI, Páez M (2016) Polyethylene/silver-nanofiber composites: a material for antibacterial films. Mater Sci Eng C 1(69):1282–1289CrossRefGoogle Scholar
  50. Zhang W, Ronca S, Mele E (2017) Electrospun nanofibres containing antimicrobial plant extracts. Nanomaterials (Basel) 7(2):E42CrossRefGoogle Scholar
  51. Zheng W, Wang Z, Song L, Zhao Q, Zhang J, Li D, Wang S, Han J, Zheng XL, Yang Z, Kong D (2012) Endothelialization and patency of RGD-functionalized vascular grafts in a rabbit carotid artery model. Biomaterials 33(10):2880–2891CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Biotechnology Division, Biology Department, Faculty of SciencesHacettepe UniversityBeytepe, AnkaraTurkey
  2. 2.Chemical Engineering and Applied Chemistry DepartmentAtilim UniversityAnkaraTurkey
  3. 3.Chemical Engineering Department and Bioengineering DivisionHacettepe UniversityBeytepe, AnkaraTurkey
  4. 4.Nanotechnology and Nanomedicine DivisionHacettepe UniversityBeytepe, AnkaraTurkey

Personalised recommendations