Biofilm Formation Reduction by Eugenol and Thymol on Biodegradable Food Packaging Material
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
CA19124
European Cooperation in Science and Technology
IGA/FT/2022/006
Tomas Bata University in Zlín
PubMed
35010130
PubMed Central
PMC8750975
DOI
10.3390/foods11010002
PII: foods11010002
Knihovny.cz E-resources
- Keywords
- antimicrobial activity, biodegradable polymers, biofilm, food packaging,
- Publication type
- Journal Article MeSH
Biofilm is a structured community of microorganisms adhering to surfaces of various polymeric materials used in food packaging. Microbes in the biofilm may affect food quality. However, the presence of biofilm can ensure biodegradation of discarded packaging. This work aims to evaluate a biofilm formation on the selected biodegradable polymer films: poly (lactic acid) (PLA), poly (butylene adipate-co-terephthalate) (PBAT), and poly (butylene succinate) (PBS) by selected bacterial strains; collection strains of Escherichiacoli, Staphylococcusaureus; and Bacillus pumilus, Bacillussubtilis, Bacillustequilensis, and Stenotrophomonasmaltophilia isolated from dairy products. Three different methods for biofilm evaluation were performed: the Christensen method, 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay, and fluorescence microscopy. High biofilm formation was confirmed on the control PBS film, whereas low biofilm formation ability was observed on the PLA polymer sample. Furthermore, the films with incorporated antimicrobial compounds (thymol or eugenol) were also prepared. Antimicrobial activity and also reduction in biofilm formation on enriched polymer films were determined. Therefore, they were all proved to be antimicrobial and effective in reducing biofilm formation. These films can be used to prepare novel active food packaging for the dairy industry to prevent biofilm formation and enhance food quality and safety in the future.
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Donlan R.M., Costerton J.W. Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms. Clin. Microbiol. Rev. 2002;15:167–193. doi: 10.1128/CMR.15.2.167-193.2002. PubMed DOI PMC
Marshall K.C., editor. Microbial Adhesion and Aggregation. 1st ed. Springer; Berlin, Heidelberg: 1984.
Li Y.-H., Tian X. Quorum Sensing and Bacterial Social Interactions in Biofilms. Sensors. 2012;12:2519–2538. doi: 10.3390/s120302519. PubMed DOI PMC
Cerca N., Pier G.B., Vilanova M., Oliveira R., Azeredo J. Quantitative analysis of adhesion and biofilm formation on hydrophilic and hydrophobic surfaces of clinical isolates of Staphylococcus epidermidis. Res. Microbiol. 2005;156:506–514. doi: 10.1016/j.resmic.2005.01.007. PubMed DOI PMC
Azeredo J., Azevedo N.F., Briandet R., Cerca N., Coenye T., Costa A.R., Desvaux M., Di Bonaventura G., Hébraud M., Jaglic Z., et al. Critical review on biofilm methods. Crit. Rev. Microbiol. 2017;43:313–351. doi: 10.1080/1040841X.2016.1208146. PubMed DOI
Shi X., Zhu X. Biofilm formation and food safety in food industries. Trends Food Sci. Technol. 2009;20:407–413. doi: 10.1016/j.tifs.2009.01.054. DOI
Bridier A., Sanchez-Vizuete P., Guilbaud M., Piard J.-C., Naïtali M., Briandet R. Biofilm-associated persistence of food-borne pathogens. Food Microbiol. 2015;45:167–178. doi: 10.1016/j.fm.2014.04.015. PubMed DOI
Wyrwa J., Barska A. Innovations in the food packaging market: Active packaging. Eur. Food Res. Technol. 2017;243:1681–1692. doi: 10.1007/s00217-017-2878-2. DOI
De Abreu D.A.P., Cruz J.M., Losada P.P. Active and Intelligent Packaging for the Food Industry. Food Rev. Int. 2012;28:146–187. doi: 10.1080/87559129.2011.595022. DOI
Yildirim S., Röcker B., Pettersen M.K., Nilsen-Nygaard J., Ayhan Z., Rutkaite R., Radusin T., Suminska P., Marcos B., Coma V. Active packaging applications for food. Compr. Rev. Food Sci. Food Saf. 2018;17:165–199. doi: 10.1111/1541-4337.12322. PubMed DOI
EC . Regulation (EC) No. 1935/2004 of the European Parliament and of the Council of 27 October 2004, on Materials and Articles Intended to Come into Contact with Food and Repealing Directives 80/509/EEC and 89/109/EEC. Volume 338. European Commission; Brussels, Belgium: 2004. pp. 4–17.
EC . Commission Regulation (EC) No. 450/2009 on Active and Intelligent Materials and Articles Intended to Come into Contact with Food. Volume 135. European Commission; Brussels, Belgium: 2009. pp. 3–11.
Beneventi E., Tietz T., Merkel S. Risk Assessment of Food Contact Materials. EFSA J. 2020;18:e181109. doi: 10.2903/j.efsa.2020.e181109. PubMed DOI PMC
Irankhah S., Ali A.A., Mallavarapu M., Soudi M.R., Subashchandrabose S.R., Gharavi S., Ayati B. Ecological role of Acinetobacter calcoaceticus GSN3 in natural biofilm formation and its advantages in bioremediation. Biofouling. 2019;35:377–391. doi: 10.1080/08927014.2019.1597061. PubMed DOI
Gu J.-D. Microbiological deterioration and degradation of synthetic polymeric materials: Recent research advances. Int. Biodeterior. Biodegrad. 2003;52:69–91. doi: 10.1016/S0964-8305(02)00177-4. DOI
Barron A., Sparks T.D. Commercial Marine-Degradable Polymers for Flexible Packaging. iScience. 2020;23:101353. doi: 10.1016/j.isci.2020.101353. PubMed DOI PMC
Vroman I., Tighzert L. Biodegradable Polymers. Materials. 2009;2:307–344. doi: 10.3390/ma2020307. DOI
Chandra R., Rustgi R. Biodegradable polymers. Prog. Polym. Sci. 1998;23:1273–1335. doi: 10.1016/S0079-6700(97)00039-7. DOI
Sharma S., Jaiswal A.K., Duffy B., Jaiswal S. Food Contact Surfaces: Challenges, Legislation and Solutions. Food Rev. Int. 2021:1–24. doi: 10.1080/87559129.2021.1929299. DOI
Sin L.T., Rahmat A.R., Rahman W.A.W.A. Handbook of Biopolymers and Biodegradable Plastics. Elsevier; Amsterdam, The Netherlands: 2013. Overview of Poly(lactic Acid) pp. 11–54. DOI
Muthuraj R., Misra M., Mohanty A.K. Hydrolytic degradation of biodegradable polyesters under simulated environmental conditions. J. Appl. Polym. Sci. 2015;132 doi: 10.1002/app.42189. DOI
Brocca D., Arvin E., Mosbæk H. Identification of organic compounds migrating from polyethylene pipelines into drinking water. Water Res. 2002;36:3675–3680. doi: 10.1016/S0043-1354(02)00084-2. PubMed DOI
Zhang H., Dudley E.G., Davidson P.M., Harte F. Critical Concentration of Lecithin Enhances the Antimicrobial Activity of Eugenol against Escherichia coli. Appl. Environ. Microbiol. 2017;83:e03467-16. doi: 10.1128/AEM.03467-16. PubMed DOI PMC
Hu Y., Du Y., Wang X., Feng T. Self-aggregation of water-soluble chitosan and solubilization of thymol as an antimicrobial agent. J. Biomed. Mater. Res. Part A. 2008;90A:874–881. doi: 10.1002/jbm.a.31871. PubMed DOI
Khayyat S.A., Roselin L.S. Recent progress in photochemical reaction on main components of some essential oils. J. Saudi Chem. Soc. 2018;22:855–875. doi: 10.1016/j.jscs.2018.01.008. DOI
Khatsee S., Daranarong D., Punyodom W., Worajittiphon P. Electrospinning polymer blend of PLA and PBAT: Electrospinnability-solubility map and effect of polymer solution parameters toward application as antibiotic-carrier mats. J. Appl. Polym. Sci. 2018;135:46486. doi: 10.1002/app.46486. DOI
Narayanan A., Neera, Mallesha, Ramana K.V. Synergized Antimicrobial Activity of Eugenol Incorporated Polyhydroxybutyrate Films Against Food Spoilage Microorganisms in Conjunction with Pediocin. Appl. Biochem. Biotechnol. 2013;170:1379–1388. doi: 10.1007/s12010-013-0267-2. PubMed DOI
CLSI . Performance Standards for Antimicrobial Disk Susceptibility Tests. 13th ed. CLSI Standard M02; Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2018.
Zanoaga M., Tanasa F. Photochemical Behavior of Multicomponent Polymeric-Based Materials; Advanced Structured Materials. Springer International Publishing; Cham, Switzerland: 2016. Photochemical Behavior of Synthetic Polymeric Multicomponent Materials Composites and Nanocomposites; pp. 109–164.
Stepanović S., Vuković D., Dakić I., Savić B., Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods. 2000;40:175–179. doi: 10.1016/S0167-7012(00)00122-6. PubMed DOI
Molecular Probes . LIVE/DEAD® BacLight Bacterial Viability Kits. Invitrogen; Waltham, MA, USA: 2004. pp. 1–8.
Ncube L.K., Ude A.U., Ogunmuyiwa E.N., Zulkifli R., Beas I.N. Environmental Impact of Food Packaging Materials: A Review of Contemporary Development from Conventional Plastics to Polylactic Acid Based Materials. Materials. 2020;13:4994. doi: 10.3390/ma13214994. PubMed DOI PMC
Galiè S., García-Gutiérrez C., Miguélez E.M., Villar C.J., Lombó F. Biofilms in the Food Industry: Health Aspects and Control Methods. Front. Microbiol. 2018;9:898. doi: 10.3389/fmicb.2018.00898. PubMed DOI PMC
Christensen G.D., Simpson W.A., Younger J.J., Baddour L.M., Barrett F.F., Melton D.M., Beachey E.H. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: A quantitative model for the adherence of staphylococci to medical devices. J. Clin. Microbiol. 1985;22:996–1006. doi: 10.1128/jcm.22.6.996-1006.1985. PubMed DOI PMC
Riss T.L. Cell Viability Assays. In: Moravec R.A., Niles A.L., Duellman S., Benink H.A., Worzella T.J., Minor L., editors. Assay Guidance Manual. Eli Lilly & Company and the National Center for Advancing Translational Sciences; Bethesda, MD, USA: 2004. pp. 357–388.
Williams S.C., Hong Y., Danavall D.C.A., Howard-Jones M.H., Gibson D., Frischer M., Verity P.G. Distinguishing between living and nonliving bacteria: Evaluation of the vital stain propidium iodide and its combined use with molecular probes in aquatic samples. J. Microbiol. Methods. 1998;32:225–236. doi: 10.1016/S0167-7012(98)00014-1. DOI
Williams G.W., Schork M.A., Brunden M.N. Basic Statistics for Quality Control in the Clinical Laboratory. CRC Crit. Rev. Clin. Lab. Sci. 1982;17:171–199. doi: 10.3109/10408368209107035. PubMed DOI
Limoli D.H., Jones C.J., Wozniak D.J. Bacterial Extracellular Polysaccharides in Biofilm Formation and Function. Microbiol. Spectr. 2015;3:1–19. doi: 10.1128/microbiolspec.MB-0011-2014. PubMed DOI PMC
Vacheethasanee K., Marchant R.E. Surfactant polymers designed to suppress bacterial (Staphylococcus epidermidis) adhesion on biomaterials. J. Biomed. Mater. Res. 2000;50:302–312. doi: 10.1002/(SICI)1097-4636(20000605)50:3<302::AID-JBM3>3.0.CO;2-1. PubMed DOI
Chen S., Peng X., Geng L., Wang H., Lin J., Chen B., Huang A. The effect of polytetrafluoroethylene particle size on the properties of biodegradable poly(butylene succinate)-based composites. Sci. Rep. 2021;11:6802. doi: 10.1038/s41598-021-86307-x. PubMed DOI PMC
Bhole Y.S., Karadkar P.B., Kharul U.K. Effect of substituent polarity, bulk, and substitution site toward enhancing gas permeation in dibromohexafluorobisphenol-a based polyarylates. J. Polym. Sci. Part B Polym. Phys. 2007;45:3156–3168. doi: 10.1002/polb.21314. DOI
Moustafa H., Guizani C., Dupont C., Martin V., Jeguirim M., Dufresne A. Utilization of Torrefied Coffee Grounds as Reinforcing Agent To Produce High-Quality Biodegradable PBAT Composites for Food Packaging Applications. ACS Sustain. Chem. Eng. 2016;5:1906–1916. doi: 10.1021/acssuschemeng.6b02633. DOI
De Matos Costa A.R., Crocitti A., de Carvalho L.H., Carroccio S.C., Cerruti P., Santagata G. Properties of Biodegradable Films Based on Poly(butylene Succinate) (PBS) and Poly(butylene Adipate-co-Terephthalate) (PBAT) Blends. Polymers. 2020;12:2317. doi: 10.3390/polym12102317. PubMed DOI PMC
Jasim S.M., Ali N.A. Properties characterization of plasticized polylactic acid /Biochar (bio carbon) nano-composites for antistatic packaging. Iraqi J. Phys. 2019;17:13–26. doi: 10.20723/ijp.17.42.13-26. DOI
Chieng B.W., Ibrahim N.A.B., Yunus W.M.Z.W., Hussein M.Z. Poly(lactic acid)/Poly(ethylene glycol) Polymer Nanocomposites: Effects of Graphene Nanoplatelets. Polymers. 2013;6:93–104. doi: 10.3390/polym6010093. DOI
Kumari S., Kumaraswamy R.V., Choudhary R.C., Sharma S.S., Pal A., Raliya R., Biswas P., Saharan V. Thymol nanoemulsion exhibits potential antibacterial activity against bacterial pustule disease and growth promotory effect on soybean. Sci. Rep. 2018;8:6650. doi: 10.1038/s41598-018-24871-5. PubMed DOI PMC
Zamani Z., Alipour D., Moghimi H.R., Mortazavi S.A.R., Saffary M. Development and Evaluation of Thymol Microparticles Using Cellulose Derivatives as Controlled Release Dosage Form. Iran. J. Pharm. Res. 2015;14:1031–1040. doi: 10.22037/IJPR.2015.1754. PubMed DOI PMC
Pramod K., Suneesh C.V., Shanavas S., Ansari S.H., Ali J. Unveiling the compatibility of eugenol with formulation excipients by systematic drug-excipient compatibility studies. J. Anal. Sci. Technol. 2015;6:34. doi: 10.1186/s40543-015-0073-2. DOI
Achinas S., Yska S.K., Charalampogiannis N., Krooneman J., Euverink G.J.W. A Technological Understanding of Biofilm Detection Techniques: A Review. Materials. 2020;13:3147. doi: 10.3390/ma13143147. PubMed DOI PMC
Ojima Y., Nunogami S., Taya M. Antibiofilm effect of warfarin on biofilm formation of Escherichia coli promoted by antimicrobial treatment. J. Glob. Antimicrob. Resist. 2016;7:102–105. doi: 10.1016/j.jgar.2016.08.003. PubMed DOI
Nguyen T., Roddick F.A., Fan L. Biofouling of Water Treatment Membranes: A Review of the Underlying Causes, Monitoring Techniques and Control Measures. Membranes. 2012;2:804–840. doi: 10.3390/membranes2040804. PubMed DOI PMC
Marcos-Zambrano L.J., Escribano P., Bouza E., Guinea J. Production of biofilm by Candida and non-Candida spp. isolates causing fungemia: Comparison of biomass production and metabolic activity and development of cut-off points. Int. J. Med Microbiol. 2014;304:1192–1198. doi: 10.1016/j.ijmm.2014.08.012. PubMed DOI
Rajamani S., Sandy R., Kota K., Lundh L., Gomba G., Recabo K., Duplantier A., Panchal R.G. Robust biofilm assay for quantification and high throughput screening applications. J. Microbiol. Methods. 2019;159:179–185. doi: 10.1016/j.mimet.2019.02.018. PubMed DOI
Hassan A., Usman J., Kaleem F., Omair M., Khalid A., Iqbal M. Evaluation of different detection methods of biofilm formation in the clinical isolates. Braz. J. Infect. Dis. 2011;15:305–311. doi: 10.1016/S1413-8670(11)70197-0. PubMed DOI
Morohoshi T., Oi T., Aiso H., Suzuki T., Okura T., Sato S. Biofilm Formation and Degradation of Commercially Available Biodegradable Plastic Films by Bacterial Consortiums in Freshwater Environments. Microbes Environ. 2018;33:332–335. doi: 10.1264/jsme2.ME18033. PubMed DOI PMC
Gzyra-Jagieła K., Sulak K., Draczyński Z., Podzimek S., Gałecki S., Jagodzińska S., Borkowski D. Modification of Poly(lactic acid) by the Plasticization for Application in the Packaging Industry. Polymers. 2021;13:3651. doi: 10.3390/polym13213651. PubMed DOI PMC
Al-Ghani M.M.A., Azzam R.A., Madkour T.M. Design and Development of Enhanced Antimicrobial Breathable Biodegradable Polymeric Films for Food Packaging Applications. Polymers. 2021;13:3527. doi: 10.3390/polym13203527. PubMed DOI PMC
Hamzah H., Pratiwi S.U.T., Hertiani T. Efficacy of Thymol and Eugenol Against Polymicrobial Biofilm. Indones. J. Pharm. 2018;29:214. doi: 10.14499/indonesianjpharm29iss4pp214. DOI
Marchese A., Barbieri R., Coppo E., Orhan I.E., Daglia M., Nabavi S.M., Izadi M., Abdollahi M., Ajami M. Antimicrobial activity of eugenol and essential oils containing eugenol: A mechanistic viewpoint. Crit. Rev. Microbiol. 2017;43:668–689. doi: 10.1080/1040841X.2017.1295225. PubMed DOI
Marchese A., Orhan I.E., Daglia M., Barbieri R., Di Lorenzo A., Nabavi S.F., Gortzi O., Izadi M. Antibacterial and antifungal activities of thymol: A brief review of the literature. Food Chem. 2016;210:402–414. doi: 10.1016/j.foodchem.2016.04.111. PubMed DOI
Memar M.Y., Raei P., Alizadeh N., Aghdam M.A., Kafil H.S. Carvacrol and thymol: Strong antimicrobial agents against resistant isolates. Rev. Med Microbiol. 2017;28:63–68. doi: 10.1097/MRM.0000000000000100. DOI
Zhang Y., Zhang Y., Zhu Z., Jiao X., Shang Y., Wen Y. Encapsulation of Thymol in Biodegradable Nanofiber via Coaxial Eletrospinning and Applications in Fruit Preservation. J. Agric. Food Chem. 2019;67:1736–1741. doi: 10.1021/acs.jafc.8b06362. PubMed DOI
Hertiani T., Utami D.T., Pratiwi S.U.T., Haniastuti T. Eugenol and thymol as potential inhibitors for polymicrobial oral biofilms: An in vitro study. J. Int. Oral Heal. 2021;13:45. doi: 10.4103/jioh.jioh_247_20. DOI
de Morais S.M., Vila-Nova N.S., Bevilaqua C., Rondon F.C., Lobo C.H., de Alencar Araripe Noronha Moura A., Sales A.D., Rodrigues A.P.R., de Figuereido J.R., Campello C.C., et al. Thymol and eugenol derivatives as potential antileishmanial agents. Bioorganic Med. Chem. 2014;22:6250–6255. doi: 10.1016/j.bmc.2014.08.020. PubMed DOI PMC
Veldhuizen E.J.A., Tjeerdsma-van Bokhoven J.L.M., Zweijtzer C., Burt S.A., Haagsman H.P. Structural Requirements for the Antimicrobial Activity of Carvacrol. J. Agric. Food Chem. 2006;54:1874–1879. doi: 10.1021/jf052564y. PubMed DOI
Adil M., Singh K., Verma P.K., Khan A.U. Eugenol-induced suppression of biofilm-forming genes in Streptococcus mutans: An approach to inhibit biofilms. J. Glob. Antimicrob. Resist. 2014;2:286–292. doi: 10.1016/j.jgar.2014.05.006. PubMed DOI
Liu D., Li H., Jiang L., Chuan Y., Yuan M., Chen H. Characterization of Active Packaging Films Made from Poly(Lactic Acid)/Poly(Trimethylene Carbonate) Incorporated with Oregano Essential Oil. Molecules. 2016;21:695. doi: 10.3390/molecules21060695. PubMed DOI PMC
Ramos M., Fortunati E., Beltrán A., Peltzer M., Cristofaro F., Visai L., Valente A.J.M., Jiménez A., Kenny J.M., Garrigós M.C. Controlled Release, Disintegration, Antioxidant, and Antimicrobial Properties of Poly (Lactic Acid)/Thymol/Nanoclay Composites. Polymers. 2020;12:1878. doi: 10.3390/polym12091878. PubMed DOI PMC
Gazzotti S., Todisco S.A., Picozzi C., Ortenzi M.A., Farina H., Lesma G., Silvani A. Eugenol-grafted aliphatic polyesters: Towards inherently antimicrobial PLA-based materials exploiting OCAs chemistry. Eur. Polym. J. 2019;114:369–379. doi: 10.1016/j.eurpolymj.2019.03.001. DOI
Chen F., Shi Z., Neoh K.G., Kang E.T. Antioxidant and antibacterial activities of eugenol and carvacrol-grafted chitosan nanoparticles. Biotechnol. Bioeng. 2009;104:30–39. doi: 10.1002/bit.22363. PubMed DOI
Husárová L., Pekařová S., Stloukal P., Kucharzcyk P., Verney V., Commereuc S., Ramone A., Koutny M. Identification of important abiotic and biotic factors in the biodegradation of poly(l-lactic acid) Int. J. Biol. Macromol. 2014;71:155–162. doi: 10.1016/j.ijbiomac.2014.04.050. PubMed DOI
Šerá J., Stloukal P., Jančová P., Verney V., Pekařová S., Koutný M. Accelerated Biodegradation of Agriculture Film Based on Aromatic–Aliphatic Copolyester in Soil under Mesophilic Conditions. J. Agric. Food Chem. 2016;64:5653–5661. doi: 10.1021/acs.jafc.6b01786. PubMed DOI
Šerá J., Serbruyns L., De Wilde B., Koutný M. Accelerated biodegradation testing of slowly degradable polyesters in soil. Polym. Degrad. Stab. 2019;171:109031. doi: 10.1016/j.polymdegradstab.2019.109031. DOI