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Efficacy of poly(lactic acid)/carvacrol electrospun membranes against Staphylococcus aureus and Candida albicans in single and mixed cultures

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Carvacrol (CAR) is one of the most promising essential oil components with antimicrobial activity. New technologies aimed to incorporate this active molecule into carrier matrix to improve the stability and prolong the biological activity. The goal of this study was to investigate the feasibility of incorporating CAR into electrospun membranes of poly(lactic acid) (PLA) for potential applications as active antimicrobial system. To this end, PLA membranes containing homogeneously dispersed CAR were successfully prepared and a series of systematic tests including morpho-mechanical properties, in vitro release rate, and antimicrobial/antibiofilm activities against Staphylococcus aureus and Candida albicans were carried out. The results revealed that CAR has a good compatibility with PLA and acts as a plasticizer, improving flexibility and extensibility of the matrix. The gradual release of CAR from PLA membranes warranted a significant antimicrobial activity up to 144 h and reduced the biofilm production by 92–96 and 88–95% of S. aureus and C. albicans in single and mixed cultures. A strong decrease of cell count, biomass, metabolic activity, and vitality of established 24- and 48-h biofilms were also demonstrated. In conclusion, this work highlights the potential of electrospun nanofibrous membranes as efficient stabilizers-carriers of CAR and opens up interesting perspectives on the use of this system as new tool for skin and wound bacterial–fungal infections.

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References

  • Abrigo M, McArthur SL, Kingshott P (2014) Electrospun nanofibers as dressings for chronic wound care: advances, challenges, and future prospects. Macromol Biosci 14:772–792

    Article  CAS  PubMed  Google Scholar 

  • Ahmad A, Khan A, Akhtar F, Yousuf S, Xess I, Khan LA, Manzoor N (2011) Fungicidal activity of thymol and carvacrol by disrupting ergosterol biosynthesis and membrane integrity against Candida. Eur J Clin Microbiol Infect Dis 30:41–50

    Article  CAS  PubMed  Google Scholar 

  • Andersen A (2006) Final report on the safety assessment of sodium p-chlorom-cresol, p-chloro-m-cresol, chlorothymol, mixed cresols, m-cresol, o-cresol, p-cresol, isopropyl cresols, thymol, o-cymen-5-ol, and carvacrol. Int J Toxicol 25(Suppl 1):29–127

    CAS  PubMed  Google Scholar 

  • Baser KHC (2008) Biological and pharmacological activities of carvacrol and carvacrol bearing essential oils. Curr Pharma Design 14:3106–3120

    Article  CAS  Google Scholar 

  • Botelho MA, Martins JG, Ruela RS, I R, Santos JA, Soares JB, França MC, Montenegro D, Ruela WS, Barros LP, Queiroz DB, Araujo RS, Sampio FC (2009) Protective effect of locally applied carvacrol gel on ligature-induced periodontitis in rats: a tapping mode AFM study. Phytother Res 23:1439–1448

    Article  CAS  PubMed  Google Scholar 

  • Chami N, Chami F, Bennis S, Trouillas J, Remmal A (2004a) Antifungal treatment with carvacrol and eugenol of oral candidiasis in immunosuppressed rats. Braz J Infect Dis 8:217–226

    Article  CAS  PubMed  Google Scholar 

  • Chami F, Chami N, Bennis S, Trouillas J, Remmal A (2004b) Evaluation of carvacrol and eugenol as prophylaxis and treatment of vaginal candidiasis in an immunosuppressed rat model. J Antimicrob Chemother 54:909–914

    Article  CAS  PubMed  Google Scholar 

  • Clinical and Laboratory Standards Institute (2008) Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard. Document M27-A3, Wayne, PA; CLSI

  • Clinical and Laboratory Standards Institute (2009) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard. Document M7-A7, Wayne, PA; CLSI

  • Dalleau S, Cateau E, Bergès T, Berjeaud JM, Imbert C (2008) In vitro activity of terpenes against Candida biofilms. Int J Antimicrob Agents 31:572–576

    Article  CAS  PubMed  Google Scholar 

  • Gaio V, Lima CA, Oliveira F, França Â, Cerca N (2017) Carvacrol is highly disruptive against coagulase-negative staphylococci in in vitro biofilms. Future Microbiol 12(Nov 23):1487–1496. https://doi.org/10.2217/fmb-2017-0122

    Article  CAS  PubMed  Google Scholar 

  • Gunal MY, Heper AO, Zaloglu N (2014) The effects of topical carvacrol application on wound healing process in male rats. Phcog J 6:10–13

    Article  CAS  Google Scholar 

  • Harriott MM, Noverr MC (2009) Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 53:3914–3922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hotaling NA, Bharti K, Kriel H, Simon CG (2015) Diameter J: a validated open source nanofiber diameter measurement tool. Biomaterials 61:327–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu X, Liu S, Zhou G, Huang Y, Xie Z, Jing X (2014) Electrospinning of polymeric nanofibers for drug delivery applications. J Control Release 185:12–21

    Article  CAS  PubMed  Google Scholar 

  • Inouye S, Takizawa T, Yamaguchi H (2001) Antibacterial activity of essential oils and their major constituents against respiratory tract pathogens by gaseous contact. J Antimicrob Chemother 47:565–573

    Article  CAS  PubMed  Google Scholar 

  • Knowles JR, Roller S, Murray DB, Naidu AS (2005) Antimicrobial action of carvacrol at different stages of dual-species biofilm development by Staphylococcus aureus and Salmonella enterica serovar Typhimurium. Appl Environ Microbiol 71:797–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landis RF, Gupta A, Lee YW, Wang LS, Golba B, Couillaud B, Ridolfo R, Das R, Rotello VM (2017) Cross-linked polymer-stabilized nanocomposites for the treatment of bacterial biofilms. ACS Nano 11:946–952

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Jung E, Yu H, Kim Y, Ha J, Kim YS, Park D (2008) Mechanisms of carvacrol-induced expression of type I collagen gene. J Dermatol Sci 52:160–169

    Article  CAS  PubMed  Google Scholar 

  • Lo Re G, Lopresti F, Petrucci G, Scaffaro R (2015) A facile method to determine pore size distribution in porous scaffold by using image processing. Micron 76:37–45

    Article  CAS  PubMed  Google Scholar 

  • Mandras N, Nostro A, Roana J, Scalas D, Banche G, Ghisetti V, Del Re S, Fucale G, Cuffini AM, Tullio V (2016) Liquid and vapour-phase antifungal activities of essential oils against Candida albicans and non-albicans Candida. BMC Complement Altern Med 16:330

    Article  PubMed  PubMed Central  Google Scholar 

  • Nair N, Biswas R, Götz F, Biswas L (2014) Impact of Staphylococcus aureus on pathogenesis in polymicrobial infections. Infect Immun 82:2162–2169

    Article  PubMed  PubMed Central  Google Scholar 

  • Nostro A, Papalia T (2012) Antimicrobial activity of carvacrol: current progress and future prospectives. Recent Pat AntiInfect Drug Discov 7:28–35

    Article  CAS  PubMed  Google Scholar 

  • Nostro A, Blanco AR, Cannatelli MA, Enea V, Flamini G, Morelli I, Sudano Roccaro A, Alonzo V (2004) Susceptibility of methicillin-resistant staphylococci to oregano essential oil, carvacrol and thymol. FEMS Microbiol Lett 230:191–195

    Article  CAS  PubMed  Google Scholar 

  • Nostro A, Sudano Roccaro A, Bisignano G, Marino A, Cannatelli MA, Pizzimenti FC, Cioni PL, Procopio F, Blanco AR (2007) Effects of oregano, carvacrol and thymol on Staphylococcus aureus and Staphylococcus epidermidis biofilms. J Med Microbiol 56:519–523

    Article  CAS  PubMed  Google Scholar 

  • Nostro A, Marino A, Blanco AR, Cellini L, Di Giulio M, Pizzimenti F, Sudano Roccaro A, Bisignano G (2009) In vitro activity of carvacrol against staphylococcal preformed biofilm by liquid and vapour contact. J Med Microbiol 58:791–797

    Article  CAS  PubMed  Google Scholar 

  • Nostro A, Scaffaro R, D’Arrigo M, Botta L, Filocamo A, Marino A, Bisignano G (2012) Study on carvacrol and cinnamaldehyde polymeric films: mechanical properties, release kinetics and antibacterial and anti-biofilm activities. Appl Microbiol Biotechnol 96:1029–1038

    Article  CAS  PubMed  Google Scholar 

  • Nostro A, Scaffaro R, D’Arrigo M, Botta L, Filocamo A, Marino A, Bisignano G (2013) Development and characterization of essential oil component-based polymer films: a potential approach to reduce bacterial biofilm. Appl Microbiol Biotechnol 97:9515–9523

    Article  CAS  PubMed  Google Scholar 

  • Nostro A, Scaffaro R, Botta L, Filocamo A, Marino A, Bisignano G (2015) Effect of temperature on the release of carvacrol and cinnamaldehyde incorporated into polymeric systems to control growth and biofilms of Escherichia coli and Staphylococcus aureus. Biofouling 31:639–649

    Article  CAS  PubMed  Google Scholar 

  • Persico P, Ambrogi V, Carfagna C, Cerruti P, Ferrocino I, Mauriello G (2009) Nanocomposite polymer films containing carvacrol for antimicrobial active packaging. Polym Engin Sci 49:1447–1455

    Article  CAS  Google Scholar 

  • Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW, Shirtliff ME (2010) Microbial interactions and differential protein expression in Staphylococcus aureus-Candida albicans dual-species biofilms. FEMS Immunol Med Microbiol 59:493–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rieger KA, Schiffman JD (2014) Electrospinning an essential oil: cinnamaldehyde enhances the antimicrobial efficacy of chitosan/poly(ethylene oxide) nanofibers. Carbohyd Polym 113:561–568

    Article  CAS  Google Scholar 

  • Scaffaro R, Lopresti F, Botta L (2017a) Preparation, characterization and hydrolytic degradation of PLA/PCL co-mingled nanofibrous mats prepared via dual-jet electrospinning. Eur Polym J 96:266–277

    Article  CAS  Google Scholar 

  • Scaffaro R, Lopresti F, Maio A, Botta L, Rigogliuso S, Ghersi G (2017b) Electrospun PCL/GO-g-PEG structures: processing-morphology-properties relationships. Compos Part A Appl Sci Manuf 92:97–107

    Article  CAS  Google Scholar 

  • Scaffaro R, Lopresti F, Sutera A, Botta L, Fontana RM, Gallo G (2017c) Plasma modified PLA electrospun membranes for actinorhodin production intensification in Streptomyces coelicolor A3(2) immobilized-cell cultivations. Colloids Surfaces B Biointerfaces 157:233–241

    Article  CAS  PubMed  Google Scholar 

  • Scaffaro R, Maio A, Lopresti F, Botta L (2017d) Nanocarbons in electrospun polymeric nanomats for tissue engineering: a review. Polymers (Basel) 9:76

    Article  Google Scholar 

  • Sokolik CG, Ben-Shabat-Binyamini R, Gedanken A, Lellouche JP (2018) Proteinaceous microspheres as a delivery system for carvacrol and thymol in antibacterial applications. Ultrason Sonochem 41:288–296

    Article  CAS  PubMed  Google Scholar 

  • Tas C, Ozkan Y, Okyar A, Savaser A (2007) In vitro and ex vivo permeation studies of etodolac from hydrophilic gels and effect of terpenes as enhancers. Drug Deliv 14:453–459

    Article  CAS  PubMed  Google Scholar 

  • Topala CM, Tataru LD (2016) ATR-FTIR study of thyme and rosemary oils extracted by supercritical carbon dioxide. Rev Chim 67:1–5

    Google Scholar 

  • Xiao L, Wang B, Yang G, Gauthier M (2012) Poly(lactic acid)-based biomaterials: synthesis, modification and applications. In Biomedical Science, Engineering and Technology. (Ed: Ghista DN) Publisher InTech, pp. 247–282

  • Yamada T, Ueda T, Ugawa S, Ishida Y, Imayasu M, Koyama S, Shimada S (2010) Functional expression of transient receptor potential vanilloid 3 (TRPV3) in corneal epithelial cells: involvement in thermosensation and wound healing. Exp Eye Res 90:121–129

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Dipartimento di Ingegneria Civile, Ambientale, Aerospaziale, dei Materiali, Viale delle Scienze Ed. 6, RU INSTM, Università di Palermo, 90128, Palermo, Italy

    Roberto Scaffaro & Francesco Lopresti

  2. Dipartimento di Scienze Chimiche, Biologiche, Farmaceutiche e Ambientali, Polo Annunziata, Università degli Studi di Messina, 98168, Messina, Italy

    Manuela D’Arrigo, Andreana Marino & Antonia Nostro

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  1. Roberto Scaffaro
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  2. Francesco Lopresti
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  3. Manuela D’Arrigo
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  4. Andreana Marino
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  5. Antonia Nostro
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Correspondence to Antonia Nostro.

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Scaffaro, R., Lopresti, F., D’Arrigo, M. et al. Efficacy of poly(lactic acid)/carvacrol electrospun membranes against Staphylococcus aureus and Candida albicans in single and mixed cultures. Appl Microbiol Biotechnol 102, 4171–4181 (2018). https://doi.org/10.1007/s00253-018-8879-7

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  • DOI: https://doi.org/10.1007/s00253-018-8879-7

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