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Antibacterial Activity of Low-Density Polyethylene and Low-Density Polyethylene-co-maleic Anhydride Films Incorporated with ZnO Nanoparticles

Abstract

This study innovatively produced polymeric active antibacterial films by incorporating zinc oxide nanoparticles (ZnO-NP) into linear low-density polyethylene grafted with maleic anhydride (LLDPE-MA) and low-density polyethylene (LDPE) using polymer melting and coating of ZnO-NP. It was evaluated the physical properties and antibacterial effects against foodborne pathogens (Staphylococcus aureus, Salmonella Typhimurium, and Pseudomonas aeruginosa) by liquid and disk-diffusion in agar tests. The active films presented 1.0, 2.5, and 5.5% of ZnO-NP. The two with higher ZnO-NP content presented similar antibacterial activity, demonstrating that the ZnO-NP availability on the film surface is more important than their total amount. Disk-diffusion in agar showed an inhibition halo for P. aeruginosa in both films with more than 5.0% in ZnO-NP, whereas for S. aureus and S. Typhimurium, the inhibition zones were not detected after 48 h. In liquid tests, P. aeruginosa was the least sensitive microorganism: from 5 log CFU/mL, it reached 9 log CFU/mL in LLDPE-MA films without ZnO-NPs and 7 log CFU/mL in films with 5.5% of ZnO-NPs after 5 days. S. Typhimurium was the most sensitive in the liquid test, with 9 log CFU/mL growth in 5 days for films without ZnO-NPs and 3 log CFU/mL for 5.5% of ZnO-NPs, in 5 days. In conclusion, ZnO-NP incorporated on LLDPE-MA and LDPE films is a promising packaging technology to increase food shelf-life and safety.

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Data Availability

The datasets generated during the current study are available from the corresponding author on reasonable request.

References

  1. Ahvenainen, R. (2003). Active and intelligent packaging: An introduction. In R. Ahvenainen (Ed.), Novel Food Packaging Techniques (pp. 5–21). Woodhead Publishing.

    Chapter  Google Scholar 

  2. Applerot, G., Lipovsky, A., Dror, R., Perkas, N., Nitzan, Y., Lubart, R., & Gedanken, A. (2009a). Enhanced antibacterial activity of nanocrystalline ZnO due to increased ROS-mediated cell injury. Advanced Functional Materials, 19(6), 842–852. https://doi.org/10.1002/adfm.200801081

    CAS  Article  Google Scholar 

  3. Applerot, G., Perkas, N., Amirian, G., Girshevitz, O., & Gedanken, A. (2009b). Coating of glass with ZnO via ultrasonic irradiation and a study of its antibacterial properties. Applied Surface Science, 256(3), S3–S8. https://doi.org/10.1016/j.apsusc.2009.04.198

    CAS  Article  Google Scholar 

  4. Aziz, S. G. G., & Almasi, H. (2018). Physical characteristics, release properties, and antioxidant and antimicrobial activities of whey protein isolate films incorporated with thyme (Thymus vulgaris L.) extract-loaded nanoliposomes. Food and Bioprocess Technology, 11(8), 1552–1565. https://doi.org/10.1007/s11947-018-2121-6

  5. Balouiri, M., Sadiki, M., & Ibnsouda, S. K. (2016). Methods for in vitro evaluating antibacterial activity: A review. Journal of Pharmaceutical Analysis, 6(2), 71–79. https://doi.org/10.1016/j.jpha.2015.11.005

    Article  PubMed  Google Scholar 

  6. Barão, M. Z. (2011). Dossiê Técnico (Embalagens para produtos alimentícios). Serviço Brasileiro de Respostas Técnicas. http://www.respostatecnica.org.br/dossie-tecnico/downloadsDT/NTY0MQ== Accessed 19 March 2021.

  7. Baughan, J. S. (2015). Future trends in global food packaging regulation, Global Legislation for Food Contact Materials. In J. S. Baughan (Ed.), Global Legislation for Food Contact Materials (pp. 65–74). Woodhead Publishing.

    Chapter  Google Scholar 

  8. Beigmohammadi, F., Peighambardoust, S. H., Hesari, J., Azadmard-Damirchi, S., Peighambardoust, S. J., & Khosrowshahi, N. K. (2016). Antibacterial properties of LDPE nanocomposite films in packaging of UF cheese. LWT - Food Science and Technology, 65, 106–111. https://doi.org/10.1016/j.lwt.2015.07.059

    CAS  Article  Google Scholar 

  9. Bumbudsanpharoke, N., Choi, J., Park, H. J., & Ko, S. (2019). Zinc migration and its effect on the functionality of a low density polyethylene-ZnO nanocomposite film. Food Packaging and Shelf Life, 20, 1–8. https://doi.org/10.1016/j.fpsl.2019.100301

    Article  Google Scholar 

  10. Carina, D., Sharma, S., Jaiswal, A. K., & Jaiswal, S. (2021). Seaweeds polysaccharides in active food packaging: A review of recent progress. Trends in Food Science & Technology, 110, 559–572. https://doi.org/10.1016/j.tifs.2021.02.022

    CAS  Article  Google Scholar 

  11. Cha, J., & White, J. L. (2001). Maleic anhydride modification of polyolefin in an experiment and kinetic model. Polymer Engineering and Science, 41(7), 1227–1237. https://doi.org/10.1002/pen.10824

    CAS  Article  Google Scholar 

  12. Chang, M. K. (2015). Mechanical properties and thermal stability of low-density polyethylene grafted maleic anhydride/montmorillonite nanocomposites. Journal of Industrial and Engineering Chemistry, 27, 96–101. https://doi.org/10.1016/j.jiec.2014.11.048

    CAS  Article  Google Scholar 

  13. Chen, C. H., Kuo, W. S., & Lai, L. S. (2013). Development of tapioca starch/decolorized hsian-tsao leaf gum-based antimicrobial films: Physical characterization and evaluation against Listeria monocytogenes. Food and Bioprocess Technology, 6(6), 1516–1525. https://doi.org/10.1007/s11947-012-0822-9

    Article  Google Scholar 

  14. Ching, K. L., Li, G., Ho, Y. L., & Kwok, H. S. (2016). The role of polarity and surface energy in the growth mechanism of ZnO from nanorods to nanotubes. CrystEngComm, 18, 779–786. https://doi.org/10.1039/C5CE02164B

    CAS  Article  Google Scholar 

  15. Emamifar, A., Kadivar, M., Shahedi, M., & Soleimanian-Zad, S. (2010). Evaluation of nanocomposite packaging containing Ag and ZnO on shelf life of fresh orange juice. Innovative Food Science and Emerging Technologies, 11(4), 742–748. https://doi.org/10.1016/j.ifset.2010.06.003

    CAS  Article  Google Scholar 

  16. Emamifar, A., Kadivar, M., Shahedi, M., & Solimanian-Zad, S. (2011). Effect of nanocomposite packaging containing Ag and ZnO on inactivation of Lactobacillus plantarum in orange juice. Journal of Food Processing and Preservation, 22(2), 408–413. https://doi.org/10.1111/j.1745-4549.2011.00558.x

    CAS  Article  Google Scholar 

  17. Eskandari, M., Haghighi, N., Ahmadi, V., Haghighi, F., & Mohammadi, S. R. (2011). Growth and investigation of antifungal properties of ZnO nanorod arrays on the glass. Physica b: Condensed Matter, 406(1), 112–114. https://doi.org/10.1016/j.physb.2010.10.035

    CAS  Article  Google Scholar 

  18. Esteban-Tejeda, L., Prado, C., Cabal, B., Sanz, J., Torrecillas, R., & Moya, J. S. (2015). Antibacterial and antifungal activity of ZnO containing glasses. PLoS ONE, 10(7), e0132709. https://doi.org/10.1371/journal.pone.0132709

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. European Commission 2016/1416 of 24 August 2016 amending and correcting Regulation (EC) No. 10/2011 on plastic materials and articles intended to come into contact with food Official Journal of the European Union, 230(22) (2016), pp. 22–42. https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32016R1416

  20. FDA (2021). Electronic Code of Federal Regulations. Title 21, Chapter I, Subchapter E, Part 582, Subpart F, §582.5991. http://www.ecfr.gov/cgi-bin/text-idx?SID=a55fc716d5afc41aaa9434cddd5e5f57&mc=true&node=se21.6.582_15991&rgn=div8. Accessed 30 March 2021.

  21. Ghule, K., Ghule, A. V., Chen, B. J., & Ling, Y. C. (2006). Preparation and characterization of ZnO nanoparticles coated paper and its antibacterial activity study. Green Chemistry, 8(12), 1034–1041. https://doi.org/10.1039/b605623g

    CAS  Article  Google Scholar 

  22. Girol, S. G., Strunskus, T., Muhler, M., Wöll, C. (2004). Reactivity of ZnO surfaces toward maleic anhydride. The Journal of Physical Chemistry B, 108, 13736–13745. https://doi.org/10.1021/jp048386d

  23. Gusatti, M., Rosário, J. A., Campos, C. E. M., Kuhnen, N. C., Carvalho, E. U., Riella, H. G., & Bernardin, A. M. (2010). Production and characterization of ZnO nanocrystals obtained by solochemical processing at different temperatures. Journal of Nanoscience and Nanotechnology, 10(7), 4348–4351. https://doi.org/10.1166/jnn.2010.2198

    CAS  Article  PubMed  Google Scholar 

  24. Hamielec, A. E., Gloor, P. E., & Zhu, S. (1991). Kinetics of free radical modification of polyolefins in extruders—chain scission, crosslinking and grafting. Journal of Chemical Engineering, 69, 611–618. https://doi.org/10.1002/cjce.5450690302

    CAS  Article  Google Scholar 

  25. Jatoi, A. W., Kim, I. S., Ogasawara, H., & Ni, Q. (2019). Characterizations and application of CA/ZnO/AgNP composite nanofibers for sustained antibacterial properties. Materials Science & Engineering C, 105, 110077. https://doi.org/10.1016/j.msec.2019.110077

    CAS  Article  Google Scholar 

  26. Jiang, Y., Zhang, L., Wen, D., & Ding, Y. (2016). Role of physical and chemical interactions in the antibacterial behavior of ZnO nanoparticles against E. coli. Materials Science and Engineering C, 69, 1361–1366. https://doi.org/10.1016/j.msec.2016.08.044

    CAS  Article  PubMed  Google Scholar 

  27. Jin, T., Sun, D., Su, J. Y., Zhang, H., & Sue, H. J. (2009). Antibacterial efficacy of zinc oxide quantum dots against Listeria monocytogenes, Salmonella Enteritidis, and Escherichia coli O157:H7. Journal of Food Science, 74(1), M46–M52. https://doi.org/10.1111/j.1750-3841.2008.01013.x

    CAS  Article  PubMed  Google Scholar 

  28. Jones, N., Ray, B., Ranjit, K. T., & Manna, A. C. (2008). Antibacterial activity of ZnO nanoparticle suspensions on a broad spectrum of microorganisms. FEMS Microbiology Letters, 279(1), 71–76. https://doi.org/10.1111/j.1574-6968.2007.01012.x

    CAS  Article  PubMed  Google Scholar 

  29. Kasemets, K., Ivask, A., Dubourguier, H. C., & Kahru, A. (2009). Toxicity of nanoparticles of ZnO, CuO and TiO2 to yeast Saccharomyces cerevisiae. Toxicology in Vitro, 23(6), 1116–1122. https://doi.org/10.1016/j.tiv.2009.05.015

    CAS  Article  PubMed  Google Scholar 

  30. Kumar, R., Umar, A., Kumar, G., & Nalwa, H. S. (2017). Antibacterial properties of ZnO nanomaterials: A review. Ceramics International, 43, 3940–3961. https://doi.org/10.1016/j.ceramint.2016.12.062

    CAS  Article  Google Scholar 

  31. Laroque, D. A., Aragão, G. M. F., Araujo, P. H. H., & Carciofi, B. A. M. (2021). Active cellulose acetate-carvacrol films: Antibacterial, physical, and thermal properties. Packaging Technology and Science, 1, 1. https://doi.org/10.1002/pts.2570

    Article  Google Scholar 

  32. Li, J. H., Hong, R. Y., Li, M. Y., Li, H. Z., Zheng, Y., & Ding, J. (2009). Effects of ZnO nanoparticles on the mechanical and antibacterial properties of polyurethane coatings. Progress in Organic Coatings, 64(4), 504–509. https://doi.org/10.1016/j.porgcoat.2008.08.013

    CAS  Article  Google Scholar 

  33. Lv, J., Fang, M., Chen, K., & Chai, Z. (2019). Thermal evolution of impurities and hydroxyl groups in ZnO nanocrystals. Journal of Luminescence, 209, 146–149. https://doi.org/10.1016/j.jlumin.2019.01.006

    CAS  Article  Google Scholar 

  34. Maniglia, B. C., Laroque, D. A., de Andrade, L. M., Carciofi, B. A. M., Tenório, J. A. S., & de Andrade, C. J. (2019). Production of active cassava starch films; effect of adding a biosurfactant or synthetic surfactant. Reactive and Functional Polymers, 144, 104368. https://doi.org/10.1016/j.reactfunctpolym.2019.104368

    CAS  Article  Google Scholar 

  35. Medeiros, G. R., Ferreira, S. R. S., & Carciofi, B. A. M. (2017). High pressure carbon dioxide for impregnation of clove essential oil in LLDPE films. Innovative Food Science & Emerging Technologies, 41, 206–215. https://doi.org/10.1016/j.ifset.2017.03.008

    CAS  Article  Google Scholar 

  36. Medeiros, G. R., Guimarães, C., Ferreira, S. R. S., & Carciofi, B. A. M. (2018). Thermomechanical and transport properties of LLDPE films impregnated with clove essential oil by high-pressure CO2. Journal of Supercritical Fluids, 139, 8–18. https://doi.org/10.1016/j.supflu.2018.05.006

    CAS  Article  Google Scholar 

  37. Mirhosseini, M., & Firouzabadi, F. B. (2013). Antibacterial activity of zinc oxide nanoparticle suspensions on foodborne pathogens. International Journal of Dairy Technology, 66(2), 291–295. https://doi.org/10.1111/1471-0307.12015

    CAS  Article  Google Scholar 

  38. Mohammadi, H., Kamkar, A., & Misaghi, A. (2018). Nanocomposite films based on CMC, okra mucilage and ZnO nanoparticles: Physico mechanical and antibacterial properties. Carbohydrate Polymers, 181, 351–357. https://doi.org/10.1016/j.carbpol.2017.10.045

    CAS  Article  PubMed  Google Scholar 

  39. Noei, H., Qiu, H., Wang, Y., Loffler, E., Woll, C., & Muhler, M. (2008). The identification of hydroxyl groups on ZnO nanoparticles by infrared spectroscopy. Physical Chemistry Chemical Physics, 10, 7092–7097. https://doi.org/10.1039/b811029h

    CAS  Article  PubMed  Google Scholar 

  40. Padmavathy, N., & Vijayaraghavan, R. (2008). Enhanced bioactivity of ZnO nanoparticles—An antibacterial study. Science and Technology of Advanced Materials, 9(3), 03 5004, https://doi.org/10.1088/1468-6996/9/3/035004

  41. Pandiyaraj, K. N., Deshmukh, R. R., Ruzybayev, I., Shah, S. I., Su, P. G., Halleluyah, M., & Halim, A. S. (2014). Influence of non-thermal plasma forming gases on improvement of surface properties of low density polyethylene (LDPE). Applied Surface Science, 307, 109–119. https://doi.org/10.1016/j.apsusc.2014.03.177

    CAS  Article  Google Scholar 

  42. Pasquet, J., Chevalier, Y., Couval, E., Bouvier, D., Noizet, G., Morlière, C., & Bolzinger, M. A. (2014). Antibacterial activity of zinc oxide particles on five microorganisms of the Challenge Tests related to their physicochemical properties. International Journal of Pharmaceutics, 460(1–2), 92–100. https://doi.org/10.1016/j.ijpharm.2013.10.031

    CAS  Article  PubMed  Google Scholar 

  43. Patil, P. P., Bohara, R. A., Meshram, J. V., Nanaware, S. G., & Pawar, S. H. (2019). Hybrid chitosan-ZnO nanoparticles coated with a sonochemical technique on silk fibroin-PVA composite film: A synergistic antibacterial activity. International Journal of Biological Macromolecules, 122, 1305–1312. https://doi.org/10.1016/j.ijbiomac.2018.09.090

    CAS  Article  PubMed  Google Scholar 

  44. Polat, S., Fenercioğlu, H., & Güçlü, M. (2018). Effects of metal nanoparticles on the physical and migration properties of low density polyethylene films. Journal of Food Engineering, 229, 32–42. https://doi.org/10.1016/j.jfoodeng.2017.12.004

    CAS  Article  Google Scholar 

  45. Porto, M. F., Girotto, E. M., Kunita, M. H., Gonçalves, M. do C., Muniz, E. C., Rubira, A. F., & Radovanovic, E. (2004). Atomic force microscopy, scanning electric potential microscopy and contact-angle surface analysis of low-density polyethylene grafted with maleic anhydride. In Surface and Colloid Science (pp. 86–91). Berlin, Heidelberg: Springer Berlin Heidelberg. https://doi.org/10.1007/b97088

  46. Prasad, V., Shaikh, A. J., Kathe, A. A., Bisoyi, D. K., Verma, A. K., & Vigneshwaran, N. (2010). Functional behaviour of paper coated with zinc oxide-soluble starch nanocomposites. Journal of Materials Processing Technology, 210(14), 1962–1967. https://doi.org/10.1016/j.jmatprotec.2010.07.009

    CAS  Article  Google Scholar 

  47. R Core Team. (2016). R: A language and environment for statistical computing. Manual, Vienna, Austria. Retrieved from http://www.r-project.org/

  48. Singer, A., Barakat, Z., Mohapatra, S., & Mohapatra, S. S. (2019). Nanoscale drug-delivery systems: In vitro and in vivo characterization. In Mohapatra, S., Ranjan, S., Dasgupta, N., Mishra, R. K., Thomas, S. (Ed.), Nano-carriers for drug delivery: nanoscience and nanotechnology in drug delivery (pp. 395–419). Amsterdam, Netherlands: Elsevier Inc. https://doi.org/10.1016/B978-0-12-814033-8.00013-8

  49. Sharma, R. K., & Ghose, R. (2015). Synthesis of zinc oxide nanoparticles by homogeneous precipitation method and its application in antifungal activity against Candida albicans. Ceramics International, 41(1), 967–975. https://doi.org/10.1016/j.ceramint.2014.09.016

    CAS  Article  Google Scholar 

  50. Sirelkhatim, A., Mahmud, S., Seeni, A., Kaus, N. H. M., Ann, L. C., Bakhori, S. K. M., & Mohamad, D. (2015). Review on zinc oxide nanoparticles: Antibacterial activity and toxicity mechanism. Nano-Micro Letters, 7(3), 219–242. https://doi.org/10.1007/s40820-015-0040-x

    CAS  Article  PubMed  Google Scholar 

  51. Song, W., Zhang, J., Guo, J., Zhang, J., Ding, F., Li, L., & Sun, Z. (2010). Role of the dissolved zinc ion and reactive oxygen species in cytotoxicity of ZnO nanoparticles. Toxicology Letters, 199(3), 389–397. https://doi.org/10.1016/j.toxlet.2010.10.003

    CAS  Article  PubMed  Google Scholar 

  52. Souza, R. C., Haberbeck, L. U., Riellla, H. G., Ribeiro, D. H. B., & Carciofi, B. A. M. (2019). Antibacterial activity of zinc oxide nanoparticles synthesized by solochemical. Brazilian Journal of Chemical Engineering, 36(2), 885–893. https://doi.org/10.1590/0104-6632.20190362s20180027

    CAS  Article  Google Scholar 

  53. Trabulsi, L. R., & Alterthum, F. (2015). Microbiologia (6th ed.). Atheneu.

    Google Scholar 

  54. Valencia-Sullca, C., Atarés, L., Vargas, M., & Chiralt, A. (2018). Physical and antimicrobial properties of compression-molded cassava starch-chitosan films for meat preservation. Food and Bioprocess Technology, 11(3), 1339–1349. https://doi.org/10.1007/s11947-018-2094-5

    CAS  Article  Google Scholar 

  55. Vicentini, D. S., Smania, A., & Laranjeira, M. C. M. (2010). Chitosan/poly (vinyl alcohol) films containing ZnO nanoparticles and plasticizers. Materials Science and Engineering C, 30(4), 503–508. https://doi.org/10.1016/j.msec.2009.01.026

    CAS  Article  Google Scholar 

  56. Xie, Y., He, Y., Irwin, P. L., Jin, T., & Shi, X. (2011). Antibacterial activity and mechanism of action of zinc oxide nanoparticles against Campylobacter jejuni. Applied and Environmental Microbiology, 77(7), 2325–2331. https://doi.org/10.1128/AEM.02149-10

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Wong, K. W. J., Field, M. R., Ou, J. Z., Latham, K., Spencer, M. J. S., Yarovsky, I., & Kalantar-zadeh, K. (2012). Interaction of hydrogen with ZnO nanopowders - Evidence of hydroxyl group formation. Nanotechnology, 23, 015705. https://doi.org/10.1088/0957-4484/23/1/015705

    CAS  Article  PubMed  Google Scholar 

  58. Yamamoto, O. (2001). Influence of particle size on the antibacterial activity of zinc oxide. International Journal of Inorganic Materials, 3(7), 643–646. https://doi.org/10.1016/S1466-6049(01)00197-0

    CAS  Article  Google Scholar 

  59. Zhang, L., Jiang, Y., Ding, Y., Povey, M., & York, D. (2007). Investigation into the antibacterial behaviour of suspensions of ZnO nanoparticles (ZnO nanofluids). Journal of Nanoparticle Research, 9(3), 479–489. https://doi.org/10.1007/s11051-006-9150-1

    CAS  Article  Google Scholar 

  60. Zhong, Q., Tian, J., Liu, T., Guo, Z., Ding, S., & Li, H. (2018). Preparation and antibacterial properties of carboxymethyl chitosan/ZnO nanocomposite microspheres with enhanced biocompatibility. Materials Letters, 212, 58–61. https://doi.org/10.1016/j.matlet.2017.10.062

    CAS  Article  Google Scholar 

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Acknowledgements

The authors thank the Kher Nanotecnologia Química Ltda, Santa Catarina, Brazil, for kindly supplying ZnO nanoparticles.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 and PRINT/CAPES-UFSC: 88887.310373/2018–00. The authors also received financial support from Laboratório Central de Microscopia Eletrônica at the Federal University of Santa Catarina (LCME-UFSC) for TEM images and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Brazil).

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Correspondence to Bruno Augusto Mattar Carciofi.

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de Souza, R.C., de Moraes, J.O., Haberbeck, L.U. et al. Antibacterial Activity of Low-Density Polyethylene and Low-Density Polyethylene-co-maleic Anhydride Films Incorporated with ZnO Nanoparticles. Food Bioprocess Technol 14, 1872–1884 (2021). https://doi.org/10.1007/s11947-021-02684-1

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Keywords

  • Food packaging
  • Food shelf-life
  • Staphylococcus aureus
  • Salmonella Typhimurium
  • Pseudomonas aeruginosa