Skip to main content
Log in

Antimicrobial nanocomposite films made of poly(lactic acid)–cellulose nanocrystals (PLA–CNC) in food applications—part B: effect of oregano essential oil release on the inactivation of Listeria monocytogenes in mixed vegetables

  • Original Paper
  • Published:
Cellulose Aims and scope Submit manuscript

Abstract

Antimicrobial nanocomposite films containing oregano essential oil (EO) were prepared by solvent casting. Film matrix was composed of supramolecular poly(lactic acid)–cellulose nanocrystals (PLA–CNC) nanocomposite. Bioactive PLA–CNC–oregano films were prepared by incorporating oregano EO as an antimicrobial agent. Resulting films were then converted into packaging applied on mixed vegetables as a food model and stored for 14 days at 4 °C to determine their antimicrobial capacity against Listeria monocytogenes, their physico-chemical/structural properties and their total phenols (TP) release during storage, in order to evaluate the effect of oregano EO. It was observed the addition of oregano EO did not affect the water vapor permeability (WVP) of films, but increased their elongation at break (Eb) and reduced their tensile strength (TS) and tensile modulus (TM) at day 0. However, TS, TM, Eb and WVP values of control and bioactive films were increased slightly after 14 days of storage. FTIR analysis allowed characterizing the molecular interactions of oregano EO with PLA–CNC matrix via the identification and interpretation of their respective vibration bands. Microbiological analysis of mixed vegetables inoculated with L. monocytogenes (3 log CFU g−1) indicated that PLA–CNC–oregano films induced a quasi-total inhibition of bacteria in vegetables at day 14 and therefore demonstrated a strong antimicrobial capacity in situ. The percentage of TP release from bioactive films was determined by Folin–Ciocalteu’s method and results showed that TP release increased continuously from day 0 to day 14, up to 16.6 % at day 14. These results allowed demonstrating the strong antimicrobial capacity of PLA–CNC–oregano films for food packaging applications in vegetable produce.

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

Access this article

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abadias M, Usall J, Anguera M, Solsona C, Vinas I (2008) Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int J Food Microbiol 123:121–129

    Article  CAS  Google Scholar 

  • Ahmad M, Benjakul S, Prodpran T, Agustini TW (2012) Physico-mechanical and antimicrobial properties of gelatin film from the skin of unicorn leather jacket incorporated with essential oils. Food Hydrocoll 28:189–199

    Article  CAS  Google Scholar 

  • ASTM (1983) Standard test method for water vapor transmission of materials. Am Soc Test Mater Method 15(09):E96

    Google Scholar 

  • ASTM (1999) Standard test method for tensile strength of plastics. Annual book of ASTM standards, ASTM international method D638–D699

  • Avila-Sosa R, Hernandez-Zamoran E, Lopez-Mendoza I, Palou E, Munguia MTJ, Nevarez-Moorillon GV, Lopez-Malo A (2010) Fungal inactivation by Mexican oregano (Limpia berlandieri Schauer) essential oil added to amaranth, chitosan, or starch edible films. J Food Sci 75:M127–M133

    Article  CAS  Google Scholar 

  • Bastarrachea L, Dhawan S, Sablani S (2011) Engineering properties of polymeric-based antimicrobial films for food packaging. Food Eng Rev 3:79–93

    Article  Google Scholar 

  • Benavides S, Carvajal VR, Reyes JE (2012) Physical, mechanical and antibacterial properties of alginate film: effect of the crosslinking degree and oregano essential oil concentration. J Food Eng 110:232–239

    Article  CAS  Google Scholar 

  • Bialka KL, Demirci A (2008) Efficacy of pulsed UV-light for the decontamination of Escherichia coli O157:H7 and Salmonella spp. on raspberries and strawberries. J Food Sci 73:201–207

    Article  Google Scholar 

  • Boumail A, Salmieri S, Klimas E, Tawema PO, Bouchard J, Lacroix M (2013) Characterization of trilayer antimicrobial diffusion films (ADFs) based on methylcellulose-polycaprolactone composites. J Agric Food Chem 61:811–821

    Article  CAS  Google Scholar 

  • Bourke P, O’Beirne D (2004) Effects of packaging type, gas atmosphere and storage temperature on survival and growth of Listeria spp. in shredded dry coleslaw and its components. Int J Food Sci Technol 39:509–523

    Article  CAS  Google Scholar 

  • Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods. Int J Food Microbiol 94:223–253

    Article  CAS  Google Scholar 

  • Del Nobile MA, Conte A, Incoronato AL, Panza O (2008) Antimicrobial efficacy and release kinetics of thymol from zein films. J Food Eng 89:57–63

    Article  Google Scholar 

  • Dorman HJD, Deans SG (2000) Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J Appl Microbiol 88:308–316

    Article  CAS  Google Scholar 

  • Edgar CD, Gray DG (2002) Influence of dextran on the phase behavior of suspensions of cellulose nanocrystals. Macromolecules 35:7400–7406

    Article  CAS  Google Scholar 

  • Elgayyar M, Draughon FA, Golden DA, Mount JR (2001) Antimicrobial activity of essential oils from plants against selected pathogenic and saprophytic microorganisms. J Food Prot 64:1019–1024

    CAS  Google Scholar 

  • Emiroglu ZK, Yemis GP, Coskun BK, Candogan K (2010) Antimicrobial activity of soy edible films incorporated with thyme and oregano essential oils on fresh ground beef patties. Meat Sci 86:283–288

    Article  CAS  Google Scholar 

  • Fabra MJ, Talens P, Chiralt A (2008) Tensile properties and water vapor permeability of sodium caseinate films containing oleic acid–beewax mixtures. J Food Eng 85:393–400

    Article  CAS  Google Scholar 

  • Fortunati E, Armentano I, Zhouc Q, Iannoni A, Saino E, Visai L, Berglund LA, Kenny JM (2012a) Multifunctional bionanocomposite films of poly(lactic acid), cellulose nanocrystals and silver nanoparticles. Carbohydr Polym 87:1596–1605

    Article  CAS  Google Scholar 

  • Fortunati E, Peltzer M, Armentano I, Torre L, Jiménez A, Kenny JM (2012b) Effects of modified cellulose nanocrystals on the barrier and migration properties of PLA nano-biocomposites. Carbohydr Polym 90:948–956

    Article  CAS  Google Scholar 

  • Gamage GR, Park HJ, Kim KM (2009) Effectiveness of antimicrobial coated oriented polypropylene/polyethylene films in sprout packaging. Food Res Int 42:832–839

    Article  CAS  Google Scholar 

  • Gonçalves CMB, Coutinho JAP, Marrucho IM (2010) Optical properties. In: Auras R, Lim L-T, Selke SEM, Tsuji H (eds) Poly(lactic acid): Synthesis, structures, properties, processing and applications. Wiley, Hoboken, NJ, pp 97–112

    Chapter  Google Scholar 

  • Gutierrez J, Rodriguez G, Barry-Ryan C, Bourke P (2008) Efficacy of plant essential oils against food-borne pathogens and spoilage bacteria associated with ready to eat vegetables: antimicrobial and sensory screening. J Food Prot 71:1846–1854

    CAS  Google Scholar 

  • Hamad W (2006) On the development and applications of cellulosic nanofibrillar and nanocrystalline materials. Can J Chem Eng 84:513–519

    Article  CAS  Google Scholar 

  • Hamad WY, Hu TQ (2010) Structure–process–yield interrelations in nanocrystalline cellulose extraction. Can J Chem Eng 88:392–402

    CAS  Google Scholar 

  • Hamad WY, Miao C (2011) Nanocomposite biomaterials of nanocrystalline cellulose (NCC) and polylactic acid (PLA). US 2011(0196094):A1

    Google Scholar 

  • Hossain KMZ, Ahmed I, Parsons AJ, Scotchford CA, Walker GS, Thielemans W, Rudd CD (2012) Physico-chemical and mechanical properties of nanocomposites prepared using cellulose nanowhiskers and poly(lactic acid). J Mater Sci 47:2675–2686

    Article  CAS  Google Scholar 

  • Hosseini MH, Razavi SH, Mousavi MA (2009) Antimicrobial, physical and mechanical properties of chitosan-based films incorporated with thyme, clove and cinnamon essential oils. J Food Process Preserv 33:727–743

    Article  CAS  Google Scholar 

  • Hughes J, Thomas R, Byun Y, Whiteside S (2012) Improved flexibility of thermally stable poly-lactic acid (PLA). Carbohydr Polym 88:165–172

    Article  CAS  Google Scholar 

  • Ippolito A, Nigro F (2003) Natural antimicrobials in postharvest storage of fresh fruits and vegetables. In: Roller S (ed) Natural antimicrobials for the minimal processing of foods. Woodhead Publishing Ltd, Cambridge, UK, pp 201–223

    Chapter  Google Scholar 

  • Iwamoto S, Kai W, Isogai A, Iwata T (2009) Elastic modulus of single cellulose microfibrils from tunicate measured by atomic force microscopy. Biomacromolecules 10:2571–2576

    Article  CAS  Google Scholar 

  • Jamshidian M, Tehrany EA, Imran M, Jacquot M, Desobry S (2010) Poly(lactic acid): Production, applications, nanocomposites, and release studies. Compr Rev Food Sci Food Saf 9:552–571

    Article  CAS  Google Scholar 

  • Jamshidian M, Tehrany EA, Imran M, Akhtar MJ, Cleymand F, Desobry S (2012) Structural, mechanical and barrier properties of active PLA–antioxidant films. J Food Eng 110:380–389

    Article  CAS  Google Scholar 

  • Johannessen GS, Loncarevic S, Kruse H (2002) Bacteriological analysis of fresh produce in Norway. Int J Food Microbiol 77:199–204

    Article  Google Scholar 

  • Johnston LM, Jaykus L-A, Moll D, Anciso J, Mora B, Moe CL (2006) A field study of the microbiological quality of fresh produce of domestic and Mexican origin. Int J Food Microbiol 112:83–95

    Article  Google Scholar 

  • Khan RA, Salmieri S, Dussault D, Calderon JU, Kamal MR, Safrany A, Lacroix M (2010) Production and properties of nanocellulose reinforced methylcellulose-based biodegradable films. J Agric Food Chem 58:7878–7879

    Article  CAS  Google Scholar 

  • Khan RA, Salmieri S, Dussault D, Sharmin N, Lacroix M (2012a) Mechanical, barrier and interfacial properties of biodegradable composite films made of methylcellulose and PCL. J Appl Polym Sci 123:1690–1697

    Article  CAS  Google Scholar 

  • Khan RA, Salmieri S, Dussault D, Uribe-Calderon J, Kamal MR, Safrany A, Lacroix M (2012b) Preparation, gamma-irradiation and thermo-mechanical characterization of chitosan-loaded methylcellulose films. J Polym Environ 20:43–52

    Article  CAS  Google Scholar 

  • Khan RA, Beck S, Dussault D, Salmieri S, Bouchard J, Lacroix M (2013) Mechanical and barrier properties of nanocrystalline cellulose-reinforced poly(caprolactone) composites: effect of gamma radiation. J Appl Polym Sci. doi:10.1002/APP.38896

    Google Scholar 

  • Klemm D, Kramer F, Moritz S, Lindstrom T, Ankerfors M, Gray D, Dorris A (2011) Nanocelluloses: a new family of nature-based materials. Angew Chem Int Ed 50:5438–5466

    Article  CAS  Google Scholar 

  • Krishnamachari P, Zhang J, Lou J, Yan J, Uitenham L (2009) Biodegradable poly(lactic acid)/clay nanocomposites by melt intercalation: a study of morphological, thermal, and mechanical properties. Int J Polym Anal Charact 14:336–350

    Article  CAS  Google Scholar 

  • Lamber RJW, Skandamis PN, Coote PJ, Nychas JE (2001) A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J Appl Microbiol 91:453–462

    Article  Google Scholar 

  • Lim L-T, Cink K, Vanyo T (2010) Processing of poly(lactic acid). In: Auras RA, Lim L-T, Selke SEM, Tsuji H (eds) Poly(lactic acid): synthesis, structures, properties, processing and applications. Wiley, Hoboken, NJ, pp 191–216

    Google Scholar 

  • Lin N, Chen G, Huang J, Dufresne A, Chang PR (2009) Effects of polymer-grafted natural nanocrystals on the structure and mechanical properties of poly(lactic acid): a case of cellulose whiskers-graft-polycaprolactone. J Appl Polym Sci 113:3417–3425

    Article  CAS  Google Scholar 

  • Lin N, Huang J, Chang PR, Feng J, Yu J (2011) Surface acetylation of cellulose nanocrystal and its reinforcing function in poly(lactic acid). Carbohydr Polym 83:1834–1842

    Article  CAS  Google Scholar 

  • Little CL, Taylor FC, Sagoo SK, Gillespie IA, Grant K, McLauchlin J (2007) Prevalence and level of Listeria monocytogenes and other Listeria species in retail pre-packaged mixed vegetable salads in the UK. Food Microbiol 24:711–717

    Article  CAS  Google Scholar 

  • López P, Sánchez C, Batlle R, Nerín C (2007) Development of flexible antimicrobial films using essential oils as active agents. J Agric Food Chem 55:8814–8824

    Article  Google Scholar 

  • Molinaro S, Romero MC, Boaro M, Sensidoni A, Lagazio C, Morris M, Kerry J (2013) Effect of nanoclay-type and PLA optical purity on the characteristics of PLA-based nanocomposite films. J Food Eng 117:113–123

    Article  CAS  Google Scholar 

  • Nhu-Trang T-T, Casabianca H, Grenier-Loustalot M-F (2006) Deuterium/hydrogen ratio analysis of thymol, carvacrol, γ-terpinene and p-cymene in thyme, savory and oregano essential oils by gas chromatography-pyrolysis-isotope ratio mass spectrometry. J Chromatogr A 1132:219–227

    Article  CAS  Google Scholar 

  • Norajit K, Kim KM, Ryu GH (2010) Comparative studies on the characterization and antioxidant properties of biodegradable alginate films containing ginseng extract. J Food Eng 98:377–384

    Article  CAS  Google Scholar 

  • Oussalah M, Caillet S, Salmieri S, Saucier L, Lacroix M (2004) Antimicrobial and antioxidant effects of milk protein-based film containing essential oils for the preservation of whole beef muscle. J Agric Food Chem 52:5598–5605

    Article  CAS  Google Scholar 

  • Oussalah M, Caillet S, Salmieri S, Saucier L, Lacroix M (2006) Antimicrobial effects of alginate-based film containing essential oils for the preservation of whole beef muscle. J Food Prot 69:2364–2369

    CAS  Google Scholar 

  • Oussalah M, Caillet S, Saucier L, Lacroix M (2007) Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Salmonella Typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control 18:414–420

    Article  CAS  Google Scholar 

  • Ozdemir M, Floros JD (2008) Optimization of edible whey protein films containing preservatives for mechanical and optical properties. J Food Eng 84:116–123

    Article  CAS  Google Scholar 

  • Ozkalp B, Sevgi F, Ozcan M, Ozcan MM (2010) The antibacterial activity of essential oil of oregano (Origanum vulgare L.). J Food Agric Environ 8:272–274

    Google Scholar 

  • Pamula E, Blazewicz M, Paluszkiewicz C, Dobrzyński P (2001) FTIR study of degradation products of aliphatic polyesters-carbon fibres composites. J Mol Struct 596:69–75

    Article  CAS  Google Scholar 

  • Pelissari F, Grossman MVE, Yamashita F, Pineda EA (2009) Antimicrobial, mechanical and barrier properties of cassava starch-chitosan films incorporated with oregano essential oil. J Agric Food Chem 57:7499–7504

    Article  CAS  Google Scholar 

  • Peng BL, Dhar N, Liu HL, Tam KC (2011) Chemistry and applications of nanocrystalline cellulose and its derivatives: a nanotechnology perspective. Can J Chem Eng 89:1191–1206

    Article  CAS  Google Scholar 

  • Rhim JW (2013) Effect of PLA lamination on performance characteristics of agar/κ-carrageenan/clay bio-nanocomposite film. Food Res Int 51:714–722

    Article  CAS  Google Scholar 

  • Rhim JW, Mohanty AK, Singh SP, Perry KWNg (2006a) Preparation and properties of biodegradable multilayer films based on soy protein isolate and poly(lactide). Ind Eng Chem Res 45:3059–3066

    Article  CAS  Google Scholar 

  • Rhim JW, Mohanty AK, Singh SP, Perry KWNg (2006b) Effect of the processing methods on the performance of polylactide films: thermocompression versus solvent casting. J Appl Polym Sci 101:3736–3742

    Article  CAS  Google Scholar 

  • Rojas-Graü MA, Avena-Bustillos RJ, Friedman M, Henika PR, Martín-Belloso O, McHugh TH (2006) Mechanical, barrier, and antimicrobial properties of apple puree edible films containing plant essential oils. J Agric Food Chem 54:9262–9267

    Article  Google Scholar 

  • Rojas-Graü MA, Avena-Bustillos RJ, Olsen C, Friedman M, Henika OR, Martín-Belloso O, Pan Z, McHugh TH (2007) Effects of plant essential oils and oils compounds on mechanical, barrier and antimicrobial properties of alginate-apple puree edible films. J Food Eng 81:634–641

    Article  Google Scholar 

  • Salmieri S, Lacroix M (2006) Physicochemical properties of alginate/polycaprolactone-based films containing essential oils. J Agric Food Chem 54:10205–10214

    Article  CAS  Google Scholar 

  • Salmieri S, Islam F, Khan RA, Hossain FM, Ibrahim HMM, Miao C, Hamad WY, Lacroix M (2014) Antimicrobial nanocomposite films made of poly(lactic acid)–cellulose nanocrystals (PLA–CNC) in food applications: part A—effect of nisin release on the inactivation of Listeria monocytogenes in ham. Cellulose 21:1837–1850

    Article  CAS  Google Scholar 

  • Samir MASA, Dufresne A (2005) Review of recent research into cellulosic whiskers, their properties and their application in nanocomposite field. Biomacromolecules 6:612–626

    Article  CAS  Google Scholar 

  • Sanchez-Gonzalez L, Vargas M, Gonzalez-Martinez C, Chiralt A, Chafer M (2011) Use of essential oils in bioactive edible coatings. Food Eng Rev 3:1–16

    Article  CAS  Google Scholar 

  • Seydim AC, Sarikus G (2006) Antimicrobial activity of whey protein based edible films incorporated with oregano, rosemary and garlic essential oils. Food Res Int 39:639–644

    Article  CAS  Google Scholar 

  • Sharmin N, Khan R, Salmieri S, Dussault D, Bouchard J, Lacroix M (2012) Mechanical and barrier properties of methylcellulose-based films grafted with trimethylolpropane trimethacrylate by gamma radiation: effect of filling with cellulose nanocrystals. JFOR 2:24–31

    Google Scholar 

  • Skandamis PN, Nychas GE (2000) Development and evaluation of a model predicting the survival of Escherichia coli O157:H7 NCTC 12900 in homemade eggplant salad at various temperatures, pHs and oregano essential oil concentrations. Appl Environ Microbiol 66:1646–1653

    Article  CAS  Google Scholar 

  • Suppakul P, Miltz J, Sonneveld K, Bigger SW (2003) Active packaging technologies with an emphasis on antimicrobial packaging and its applications. J Food Sci 68:408–420

    Article  CAS  Google Scholar 

  • Theinsathid P, Visessanguan W, Kingcha Y, Keeratipibul S (2011) Antimicrobial effectiveness of biobased film against Escherichia coli 0157:H7, Listeria monocytogenes and Salmonella Typhimurium. Adv J Food Sci Technol 3:294–302

    Google Scholar 

  • Zinoviadou K, Koutsoumanis KP, Biliaderis C (2009) Physico-chemical properties of whey protein isolate films containing oregano oil and their antimicrobial action against spoilage flora of fresh beef. Meat Sci 82:338–345

    Article  CAS  Google Scholar 

  • Zivanovic S, Chi S, Draughon AF (2005) Antimicrobial activity of chitosan films enriched with essential oils. J Food Sci 70:M45–M51

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported under a research agreement with ArboraNano Inc. (Pointe-Claire, QC, Canada). Thanks to Winpak Division Ltd for providing packaging. Special thanks go to FPInnovations for their generous contribution to provide PLA–CNC nanocomposite material.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Wadood Y. Hamad or Monique Lacroix.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Salmieri, S., Islam, F., Khan, R.A. et al. Antimicrobial nanocomposite films made of poly(lactic acid)–cellulose nanocrystals (PLA–CNC) in food applications—part B: effect of oregano essential oil release on the inactivation of Listeria monocytogenes in mixed vegetables. Cellulose 21, 4271–4285 (2014). https://doi.org/10.1007/s10570-014-0406-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10570-014-0406-0

Keywords

Navigation