Abstract
The aim of the present study was to produce lactoferrin (L) and chitosan (C) nanoparticles by ionic cross-linking with TPP and thereby increase the antimicrobial activity of biopolymers. The nanoparticles were synthesized in different proportions of biopolymers and TPP and characterized regarding their size, zeta potential, morphology, chemical interactions, structural characteristics, and antibacterial activity. They were also applied as coatings on strawberries with the aim of increasing fruit shelf-life. Circular dichroism spectra revealed that the addition of TPP altered the secondary structure of lactoferrin. The nanoparticles 3.5L:5.5C:1TPP and 4.5L:4.5C:1TPP showed higher zeta potential values and lower hydrodynamic diameters (+39.30 mV, 81.87 nm and +33.07 mV, 97.67 nm, respectively) and intense bacteriostatic action against S. aureus (0.0370 mg/ml and 0.0463 mg/ml, respectively). The minimum inhibitory concentration of these nanoparticles was three times lower than those of pure biopolymers. When applied to strawberries coating, the nanoparticles delayed the ripening and degradation of the fruit. These results confirm that it is possible to intensify the antimicrobial properties of lactoferrin and chitosan through ionic cross-linking with TPP and, thus, expand their use as natural food preservatives.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Abd El-Hack, M. E., El-Saadony, M. T., Shafi, M. E., Zabermawi, N. M., Arif, M., Batiha, G. E., Khafaga, A. F., Abd El-Hakim, Y. M., & Al-Sagheer, A. A. (2020). Antimicrobial and antioxidant properties of chitosan and its derivatives and their applications: A review. International Journal of Biological Macromolecules, 164, 2726–2744. https://doi.org/10.1016/J.IJBIOMAC.2020.08.153
Abdelhamid, A. G., & El-Dougdoug, N. K. (2020). Controlling foodborne pathogens with natural antimicrobials by biological control and antivirulence strategies. Heliyon, 6(9), e05020. https://doi.org/10.1016/J.HELIYON.2020.E05020
Ahmad, N., Wee, C. E., Wai, L. K., Zin, N. M., & Azmi, F. (2021). Biomimetic amphiphilic chitosan nanoparticles: Synthesis characterization and antimicrobial activity. Carbohydrate Polymers, 254, 117299. https://doi.org/10.1016/j.carbpol.2020.117299
Alhalwani, A. Y., Davey, R. L., Kaul, N., Barbee, S. A., & Alex Huffman, J. (2019). Modification of lactoferrin by peroxynitrite reduces its antibacterial activity and changes protein structure. Proteins: Structure, Function, and Bioinformatics, 88(1), 166–174. https://doi.org/10.1002/prot.25782
Amjadi, S., Emaminia, S., Nazari, M., Davudian, S. H., Roufegarinejad, L., & Hamishehkar, H. (2019). Application of reinforced ZnO nanoparticle-incorporated gelatin bionanocomposite film with chitosan nanofiber for packaging of chicken fillet and cheese as food models. Food and Bioprocess Technology, 12(7), 1205–1219. https://doi.org/10.1007/s11947-019-02286-y
Antoniou, J., Liu, F., Majeed, H., Qi, J., Yokoyama, W., & Zhong, F. (2015). Physicochemical and morphological properties of size-controlled chitosan–tripolyphosphate nanoparticles. Colloids and Surfaces a: Physicochemical and Engineering Aspects, 465, 137–146. https://doi.org/10.1016/J.COLSURFA.2014.10.040
Apurva, M., & Mazumdar, H. (2020). Predicting structural class for protein sequences of 40% identity based on features of primary and secondary structure using Random Forest algorithm. Computational Biology and Chemistry, 84, 107164. https://doi.org/10.1016/J.COMPBIOLCHEM.2019.107164
Assadpour, E., & Jafari, S. M. (2019). Advances in spray-drying encapsulation of food bioactive ingredients: From microcapsules to nanocapsules. Annual Review of Food Science and Technology, 10, 103–131. https://doi.org/10.1146/ANNUREV-FOOD-032818-121641
Azlin-Hasim, S., Cruz-Romero, M. C., Morris, M. A., Padmanabhan, S. C., Cummins, E., & Kerry, J. P. (2016). The potential application of antimicrobial silver polyvinyl chloride nanocomposite films to extend the shelf-life of chicken breast fillets. Food and Bioprocess Technology, 9(10), 1661–1673. https://doi.org/10.1007/s11947-016-1745-7
Bahrami, A., Delshadi, R., Jafari, S. M., & Williams, L. (2019). Nanoencapsulated nisin: An engineered natural antimicrobial system for the food industry. Trends in Food Science & Technology, 94, 20–31. https://doi.org/10.1016/J.TIFS.2019.10.002
Baker, E. N., & Baker, H. M. (2009). A structural framework for understanding the multifunctional character of lactoferrin. Biochimie, 91(1), 3–10. https://doi.org/10.1016/j.biochi.2008.05.006
Bashir, H. A., & Abu-Goukh, A. B. A. (2003). Compositional changes during guava fruit ripening. Food Chemistry, 80(4), 557–563. https://doi.org/10.1016/S0308-8146(02)00345-X
Becaro, A. A., Puti, F. C., Panosso, A. R., Gern, J. C., Brandão, H. M., Correa, D. S., & Ferreira, M. D. (2016). Postharvest quality of fresh-cut carrots packaged in plastic films containing silver nanoparticles. Food and Bioprocess Technology, 9(4), 637–649. https://doi.org/10.1007/s11947-015-1656-z
Bellamy, W., Takase, M., Yamauchi, K., Wakabayashi, H., Kawase, K., & Tomita, M. (1992). Identification of the bactericidal domain of lactoferrin. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1121(1–2), 130–136. https://doi.org/10.1016/0167-4838(92)90346-F
Benltoufa, S., Miled, W., Trad, M., Slama, R. B., & Fayala, F. (2020). Chitosan hydrogel-coated cellulosic fabric for medical end-use: Antibacterial properties, basic mechanical and comfort properties. Carbohydrate Polymers, 227, 115352. https://doi.org/10.1016/J.CARBPOL.2019.115352
Bhardwaj, S., Bhardwaj, N. K., & Negi, Y. S. (2021). Surface coating of chitosan of different degree of acetylation on non surface sized writing and printing grade paper. Carbohydrate Polymers, 269, 117674. https://doi.org/10.1016/J.CARBPOL.2021.117674
Biernbaum, E. N., Gnezda, A., Akbar, S., Franklin, R., Venturelli, P. A., & McKillip, J. L. (2021). Lactoferrin as an antimicrobial against Salmonella enterica and Escherichia coli O157:H7 in raw milk. JDS Communications, 2(3), 92–97. https://doi.org/10.3168/JDSC.2020-0030
Calvo, P., Remuñán-López, C., Vila-Jato, J. L., & Alonso, M. J. (1997). Novel hydrophilic chitosan-polyethylene oxide nanoparticles as protein carriers. Journal of Applied Polymer Science, 63(1), 125–132. https://doi.org/10.1002/(SICI)1097-4628(19970103)63:1%3c125::AID-APP13%3e3.0.CO;2-4
Campos, C. A., Gerschenson, L. N., & Flores, S. K. (2011). Development of edible films and coatings with antimicrobial activity. Food and Bioprocess Technology, 4(6), 849–875. https://doi.org/10.1007/s11947-010-0434-1
Castelo Branco Melo, N. F., de Mendonça Soares, B. L., Marques Diniz, K., Ferreira Leal, C., Canto, D., Flores, M. A. P., Henriqueda Costa Tavares-Filho, J., Galembeck, A., Montenegro Stamford, T. L., Montenegro Stamford-Arnaud, T., & Montenegro Stamford, T. C. (2018). Effects of fungal chitosan nanoparticles as eco-friendly edible coatings on the quality of postharvest table grapes. Postharvest Biology and Technology, 139, 56–66. https://doi.org/10.1016/J.POSTHARVBIO.2018.01.014
Castro-Rosas, J., Ferreira-Grosso, C. R., Gómez-Aldapa, C. A., Rangel-Vargas, E., Rodríguez-Marín, M. L., Guzmán-Ortiz, F. A., & Falfan-Cortes, R. N. (2017). Recent advances in microencapsulation of natural sources of antimicrobial compounds used in food - A review. Food Research International, 102, 575–587. https://doi.org/10.1016/J.FOODRES.2017.09.054
Chaparro, S. C. V., Tatiana, J., Salguero, V., Martínez Baquero, D. A., & Rosas Pérez, J. E. (2018). Effect of polyvalence on the antibacterial activity of a synthetic peptide derived from bovine lactoferricin against healthcare-associated infectious pathogens. BioMed Research International, 2018, 5252891. https://doi.org/10.1155/2018/5252891
Chen, W. S., & Soucie, W. G. (1986). The ionic modification of the surface charge and isoelectric point of soy protein. Journal of the American Oil Chemists’ Society, 63(10), 1346–1350. https://doi.org/10.1007/BF02679599
Ciursă, P., Pauliuc, D., Dranca, F., Ropciuc, S., & Oroian, M. (2021). Detection of honey adulterated with agave, corn, inverted sugar, maple and rice syrups using FTIR analysis. Food Control, 130, 108266. https://doi.org/10.1016/J.FOODCONT.2021.108266
de Carvalho, F. G., Magalhães, T. C., Teixeira, N. M., Gondim, B. L. C., Carlo, H. L., dos Santos, R. L., de Oliveira, A. R., & Denadai, Â. M. L. (2019). Synthesis and characterization of TPP/chitosan nanoparticles: Colloidal mechanism of reaction and antifungal effect on C. albicans biofilm formation. Materials Science and Engineering C, 104, 109885. https://doi.org/10.1016/j.msec.2019.109885
Delshadi, R., Bahrami, A., Assadpour, E., Williams, L., & Jafari, S. M. (2021). Nano/microencapsulated natural antimicrobials to control the spoilage microorganisms and pathogens in different food products. Food Control, 128, 108180. https://doi.org/10.1016/J.FOODCONT.2021.108180
Díaz-Mula, H. M., Serrano, M., & Valero, D. (2012). Alginate coatings preserve fruit quality and bioactive compounds during storage of sweet cherry fruit. Food and Bioprocess Technology, 5(8), 2990–2997. https://doi.org/10.1007/S11947-011-0599-2
Divya, K., Vijayan, S., George, T. K., & Jisha, M. S. (2017). Antimicrobial properties of chitosan nanoparticles: Mode of action and factors affecting activity. Fibers and Polymers, 18(2), 221–230. https://doi.org/10.1007/S12221-017-6690-1
Duarte, L. G. R., Alencar, W. M. P., Iacuzio, R., Silva, N. C. C., & Picone, C. S. F. (2022). Synthesis, characterization and application of antibacterial lactoferrin nanoparticles. Current Research in Food Science, 5, 642–652. https://doi.org/10.1016/J.CRFS.2022.03.009
Duarte, L. G. R., & Picone, C. S. F. (2022). Antimicrobial activity of lactoferrin-chitosan-gellan nanoparticles and their influence on strawberry preservation. Food Research International, 159, 111586. https://doi.org/10.1016/J.FOODRES.2022.111586
Duca, G., Anghel, L., & Erhan, R. V. (2018). Structural aspects of lactoferrin and serum transferrin observed by ftir spectroscopy. Chemistry Journal of Moldova: General, Industrial and Ecological Chemistry, 13(1), 111–116. https://doi.org/10.19261/cjm.2018.482
Eshghi, S., Hashemi, M., Mohammadi, A., Badii, F., Mohammadhoseini, Z., & Ahmadi, K. (2014). Effect of nanochitosan-based coating with and without copper loaded on physicochemical and bioactive components of fresh strawberry fruit (Fragaria x ananassa Duchesne) during storage. Food and Bioprocess Technology, 7(8), 2397–2409. https://doi.org/10.1007/s11947-014-1281-2
Espitia, P. J. P., de Fátima Ferreira Soares, N., Séliados Reis Coimbra, J., Joséde Andrade, N., Souza Cruz, R., & Antonio Alves Medeiros, E. (2012). Zinc oxide nanoparticles: Synthesis, antimicrobial activity and food packaging applications. Food and Bioprocess Technology, 5(5), 1447–1464. https://doi.org/10.1007/s11947-012-0797-6
Fan, C., Huang, Y. Z., Lin, J. N., & Li, J. (2021). Microplastic constituent identification from admixtures by Fourier-transform infrared (FTIR) spectroscopy: The use of polyethylene terephthalate (PET), polyethylene (PE), polypropylene (PP), polyvinyl chloride (PVC) and nylon (NY) as the model constituents. Environmental Technology & Innovation, 23, 101798. https://doi.org/10.1016/J.ETI.2021.101798
Ferreira, C. D., & Nunes, I. L. (2019). Oil nanoencapsulation: Development, application, and incorporation into the food market. Nanoscale Research Letters, 14(1), 1–13. https://doi.org/10.1186/S11671-018-2829-2
Ferreira, D. F. (2019). Sisvar: A computer analysis system to fixed effects split plot type designs. Revista Brasileira de Biometria, 37(4), 529–535. https://doi.org/10.28951/RBB.V37I4.450
Gao, Y., Xu, D., Ren, D., Zeng, K., & Wu, X. (2020). Green synthesis of zinc oxide nanoparticles using Citrus sinensis peel extract and application to strawberry preservation: A comparison study. LWT, 126, 109297. https://doi.org/10.1016/J.LWT.2020.109297
García-Otero, X., Díaz-Tome, V., Regueiro, U., Lo, M., Gonzaíez-Barcia, M., Isabel Lema, M., & Javier Otero-Espinar, F. (2021). Design, optimization, and characterization of lactoferrin-loaded chitosan/tpp and chitosan/sulfobutylether-β-cyclodextrin nanoparticles as a pharmacological alternative for keratoconus treatment. ACS Applied Materials & Interfaces, 13, 3575. https://doi.org/10.1021/acsami.0c18926
Goy, R. C., Morais, S. T. B., & Assis, O. B. G. (2016). Evaluation of the antimicrobial activity of chitosan and its quaternized derivative on E. coli and S. aureus growth. Revista Brasileira de Farmacognosia, 26(1), 122–127. https://doi.org/10.1016/j.bjp.2015.09.010
Gutiérrez-Molina, J., Corona-Rangel, M. L., Ventura-Aguilar, R. I., Barrera-Necha, L. L., Bautista-Baños, S., & Correa-Pacheco, Z. N. (2021). Chitosan and Byrsonima crassifolia-based nanostructured coatings: Characterization and effect on tomato preservation during refrigerated storage. Food Bioscience, 42, 101212. https://doi.org/10.1016/J.FBIO.2021.101212
Hadidi, M., Jafarzadeh, S., & Ibarz, A. (2021). Modified mung bean protein: Optimization of microwave-assisted phosphorylation and its functional and structural characterizations. LWT, 151, 112119. https://doi.org/10.1016/J.LWT.2021.112119
Harouna, S., Franco, I., Carramiñana, J. J., Blázquez, A., Abad, I., Pérez, M. D., Calvo, M., & Sánchez, L. (2020). Effect of hydrolysis and microwave treatment on the antibacterial activity of native bovine milk lactoferrin against Cronobacter sakazakii. International Journal of Food Microbiology, 319, 108495. https://doi.org/10.1016/J.IJFOODMICRO.2019.108495
Hashemi, S. M. B., & Jafarpour, D. (2020). Fermentation of bergamot juice with Lactobacillus plantarum strains in pure and mixed fermentations: Chemical composition, antioxidant activity and sensorial properties. LWT, 131, 109803. https://doi.org/10.1016/J.LWT.2020.109803
Håversen, L., Kondori, N., Baltzer, L., Hanson, L. Å., Dolphin, G. T., Dunér, K., & Mattsby-Baltzer, I. (2010). Structure-microbicidal activity relationship of synthetic fragments derived from the antibacterial α-helix of human lactoferrin. Antimicrobial Agents and Chemotherapy, 54(1), 418–425. https://doi.org/10.1128/AAC.00908-09
He, X., Fu, P., Aker, W. G., & Hwang, H. M. (2018). Toxicity of engineered nanomaterials mediated by nano–bio–eco interactions. Journal of Environmental Science and Health, Part C, 36(1), 21–42. https://doi.org/10.1080/10590501.2017.1418793
Hochella, M. F., Mogk, D. W., Ranville, J., Allen, I. C., Luther, G. W., Marr, L. C., McGrail, B. P., Murayama, M., Qafoku, N. P., Rosso, K. M., Sahai, N., Schroeder, P. A., Vikesland, P., Westerhoff, P., & Yang, Y. (2019). Natural, incidental, and engineered nanomaterials and their impacts on the Earth system. Science, 363(6434), eaau8299. https://doi.org/10.1126/SCIENCE.AAU8299
Hosseini, H., Tajiani, Z., & Jafari, S. M. (2019). Improving the shelf-life of food products by nano/micro-encapsulated ingredients. Food Quality and Shelf Life (pp. 159–200). Academic Press. https://doi.org/10.1016/B978-0-12-817190-5.00005-7
Howell, N. K. (1992). Protein-protein interactions. Biochemistry of Food Proteins (pp. 35–74). Springer. https://doi.org/10.1007/978-1-4684-9895-0_2
Jin, H., Li, P., Jin, Y., & Sheng, L. (2021). Effect of sodium tripolyphosphate on the interaction and aggregation behavior of ovalbumin-lysozyme complex. Food Chemistry, 352, 129457. https://doi.org/10.1016/J.FOODCHEM.2021.129457
Kaur, R., & Kaur, L. (2021). Encapsulated natural antimicrobials: A promising way to reduce microbial growth in different food systems. Food Control, 123, 107678. https://doi.org/10.1016/J.FOODCONT.2020.107678
Khoerunnisa, F., Nurhayati, M., Dara, F., Rizki, R., Nasir, M., Aji Aziz, H., Hendrawan, H., Poh, N. E., Kaewsaneha, C., & Opaprakasit, P. (2021). Physicochemical properties of TPP-crosslinked chitosan nanoparticles as potential antibacterial agents. Fibers and Polymers, 22(11), 2954–2964. https://doi.org/10.1007/s12221-021-0397-z
Koshani, R., & Jafari, S. M. (2019). Ultrasound-assisted preparation of different nanocarriers loaded with food bioactive ingredients. Advances in Colloid and Interface Science, 270, 123–146. https://doi.org/10.1016/J.CIS.2019.06.005
Kritchenkov, A. S., Egorov, A. R., Dubashynskaya, N. V., Volkova, O. V., Zabodalova, L. A., Suchkova, E. P., Kurliuk, A. V., Shakola, T. V., & Dysin, A. P. (2019). Natural polysaccharide-based smart (temperature sensing) and active (antibacterial, antioxidant and photoprotective) nanoparticles with potential application in biocompatible food coatings. International Journal of Biological Macromolecules, 134, 480–486. https://doi.org/10.1016/J.IJBIOMAC.2019.04.194
Leiva, W., Toro, N., Robles, P., Gálvez, E., & Jeldres, R. I. (2021). Use of multi-anionic sodium tripolyphosphate to enhance dispersion of concentrated kaolin slurries in seawater. Metals, 11(7), 1085. https://doi.org/10.3390/met11071085
Li, D., Zhang, X., Li, L., Aghdam, M. S., Wei, X., Liu, J., Xu, Y., & Luo, Z. (2019a). Elevated CO2 delayed the chlorophyll degradation and anthocyanin accumulation in postharvest strawberry fruit. Food Chemistry, 285, 163–170. https://doi.org/10.1016/J.FOODCHEM.2019.01.150
Li, D., Zhang, X., Xu, Y., Li, L., Aghdam, M. S., & Luo, Z. (2019b). Effect of exogenous sucrose on anthocyanin synthesis in postharvest strawberry fruit. Food Chemistry, 289, 112–120. https://doi.org/10.1016/J.FOODCHEM.2019.03.042
Linklater, D. P., Baulin, V. A., Le Guével, X., Fleury, J. -B., Hanssen, E., Hong Phong Nguyen, T., Juodkazis, S., Bryant, G., Crawford, R. J., Stoodley, P., Ivanova, E. P., Linklater, D. P., Bryant, G., Crawford, R. J., Ivanova, E. P., Juodkazis, S., Baulin, V. A., Guével, X. L., Fleury, J., & Stoodley, P. (2020). Antibacterial Action of Nanoparticles by Lethal Stretching of Bacterial Cell Membranes. Advanced Materials, 32, 2005679. https://doi.org/10.1002/adma.202005679
Liu, F., Zhang, S., Li, J., McClements, D. J., & Liu, X. (2018). Recent development of lactoferrin-based vehicles for the delivery of bioactive compounds: Complexes emulsions and nanoparticles. Trends in Food Science & Technology, 79, 67–77. https://doi.org/10.1016/j.tifs.2018.06.013
Luo, Y., Zhang, B., Cheng, W. H., & Wang, Q. (2010). Preparation, characterization and evaluation of selenite-loaded chitosan/TPP nanoparticles with or without zein coating. Carbohydrate Polymers, 82(3), 942–951. https://doi.org/10.1016/j.carbpol.2010.06.029
Maciel, K. S., Santos, L. S., Bonomo, R. C. F., Verissimo, L. A. A., Minim, V. P. R., & Minim, L. A. (2020). Purification of lactoferrin from sweet whey using ultrafiltration followed by expanded bed chromatography. Separation and Purification Technology, 251, 117324. https://doi.org/10.1016/J.SEPPUR.2020.117324
Maillard, J. -Y., & Hartemann, P. (2013). Silver as an antimicrobial: Facts and gaps in knowledge. Critical Reviews in Microbiology, 39(4), 373–383. https://doi.org/10.3109/1040841X.2012.713323
Maqbool, M., Ali, A., Alderson, P. G., Mohamed, M. T. M., Siddiqui, Y., & Zahid, N. (2011). Postharvest application of gum arabic and essential oils for controlling anthracnose and quality of banana and papaya during cold storage. Postharvest Biology and Technology, 62(1), 71–76. https://doi.org/10.1016/J.POSTHARVBIO.2011.04.002
Mauricio-Sánchez, R. A., Salazar, R., Luna-Bárcenas, J. G., & Mendoza-Galván, A. (2018). FTIR spectroscopy studies on the spontaneous neutralization of chitosan acetate films by moisture conditioning. Vibrational Spectroscopy, 94, 1–6. https://doi.org/10.1016/J.VIBSPEC.2017.10.005
McClements, D. J. (2011). Edible nanoemulsions: Fabrication, properties, and functional performance. Soft Matter, 7(6), 2297–2316. https://doi.org/10.1039/C0SM00549E
Miles, A. J., Janes, R. W., & Wallace, B. A. (2021). Tools and methods for circular dichroism spectroscopy of proteins: A tutorial review. Chemical Society Reviews, 50(15), 8400–8413. https://doi.org/10.1039/D0CS00558D
Miles, A. J., Ramalli, S. G., & Wallace, B. A. (2022). DichroWeb, a website for calculating protein secondary structure from circular dichroism spectroscopic data. Protein Science, 31(1), 37–46. https://doi.org/10.1002/PRO.4153
Miles, A. J., & Wallace, B. A. (2006). Synchrotron radiation circular dichroism spectroscopy of proteins and applications in structural and functional genomics. Chemical Society Reviews, 35(1), 39–51. https://doi.org/10.1039/B316168B
Mohamed, N., & Madian, N. G. (2020). Evaluation of the mechanical, physical and antimicrobial properties of chitosan thin films doped with greenly synthesized silver nanoparticles. Materials Today Communications, 25, 101372. https://doi.org/10.1016/J.MTCOMM.2020.101372
Mousavi, S. A., Ghotaslou, R., Kordi, S., Khoramdel, A., Aeenfar, A., Kahjough, S. T., & Akbarzadeh, A. (2018). Antibacterial and antifungal effects of chitosan nanoparticles on tissue conditioners of complete dentures. International Journal of Biological Macromolecules, 118, 881–885. https://doi.org/10.1016/J.IJBIOMAC.2018.06.151
Müller, R. H., Jacobs, C., & Kayser, O. (2001). Nanosuspensions as particulate drug formulations in therapy: Rationale for development and what we can expect for the future. Advanced Drug Delivery Reviews, 47(1), 3–19. https://doi.org/10.1016/S0169-409X(00)00118-6
Nakamura, M., Tsuda, N., Miyata, T., & Ikenaga, M. (2022). Antimicrobial effect and mechanism of bovine lactoferrin against the potato common scab pathogen Streptomyces scabiei. PLoS ONE, 17(2), e0264094. https://doi.org/10.1371/JOURNAL.PONE.0264094
Niaz, B., Saeed, F., Ahmed, A., Imran, M., Maan, A. A., Khan, M. K. I., Tufail, T., Anjum, F. M., Hussain, S., & Suleria, H. A. R. (2019). Lactoferrin (LF): A natural antimicrobial protein. International Journal of Food Properties, 22(1), 1626–1641. https://doi.org/10.1080/10942912.2019.1666137
Pan, C., Qian, J., Zhao, C., Yang, H., Zhao, X., & Guo, H. (2020). Study on the relationship between crosslinking degree and properties of TPP crosslinked chitosan nanoparticles. Carbohydrate Polymers, 241, 116349. https://doi.org/10.1016/J.CARBPOL.2020.116349
Parreidt, T. S., Lindner, M., Rothkopf, I., Schmid, M., & Müller, K. (2019). The development of a uniform alginate-based coating for cantaloupe and strawberries and the characterization of water barrier properties. Foods, 8(6), 203. https://doi.org/10.3390/FOODS8060203
Perinelli, D. R., Fagioli, L., Campana, R., Lam, J. K. W., Baffone, W., Palmieri, G. F., Casettari, L., & Bonacucina, G. (2018). Chitosan-based nanosystems and their exploited antimicrobial activity. European Journal of Pharmaceutical Sciences, 117, 8–20. https://doi.org/10.1016/J.EJPS.2018.01.046
Poverenov, E., Rutenberg, R., Danino, S., Horev, B., & Rodov, V. (2014). Gelatin-chitosan composite films and edible coatings to enhance the quality of food products: layer-by-layer vs. blended formulations. Food and Bioprocess Technology, 7(11), 3319–3327. https://doi.org/10.1007/s11947-014-1333-7
Rana, S., Siddiqui, S., & Goyal, A. (2015). Extension of the shelf life of guava by individual packaging with cling and shrink films. Journal of Food Science and Technology, 52(12), 8148–8155. https://doi.org/10.1007/S13197-015-1881-5/TABLES/5
Rezaei, A., Fathi, M., & Jafari, S. M. (2019). Nanoencapsulation of hydrophobic and low-soluble food bioactive compounds within different nanocarriers. Food Hydrocolloids, 88, 146–162. https://doi.org/10.1016/J.FOODHYD.2018.10.003
Rinaudo, M., & Domard, A. (1989). Chitin and chitosan. Sources, chemistry, biochemistry, physical properties and applications. Elsevier.
Robledo, N., López, L., Bunger, A., Tapia, C., & Abugoch, L. (2018). Effects of antimicrobial edible coating of thymol nanoemulsion/quinoa protein/chitosan on the safety, sensorial properties, and quality of refrigerated strawberries (Fragaria × ananassa) under commercial storage environment. Food and Bioprocess Technology, 11(8), 1566–1574. https://doi.org/10.1007/s11947-018-2124-3
Sampathkumar, K., Tan, K. X., & Loo, S. C. J. (2020). Developing nano-delivery systems for agriculture and food applications with nature-derived polymers. Iscience, 23(5), 101055. https://doi.org/10.1016/J.ISCI.2020.101055
Santos, M. B., Geraldo de Carvalho, M., & Garcia-Rojas, E. E. (2021). Carboxymethyl tara gum-lactoferrin complex coacervates as carriers for vitamin D3: Encapsulation and controlled release. Food Hydrocolloids, 112, 106347. https://doi.org/10.1016/J.FOODHYD.2020.106347
Saraiva, C. S., dos Reis Coimbra, J. S., de Carvalho Teixeira, A. V. N., de Oliveira, E. B., Teófílo, R. F., da Costa, A. R., & de Almeida Alves Barbosa, E. (2017). Formation and characterization of supramolecular structures of β-lactoglobulin and lactoferrin proteins. Food Research International, 100, 674–681. https://doi.org/10.1016/J.FOODRES.2017.07.065
Shankar, S., Khodaei, D., & Lacroix, M. (2021). Effect of chitosan/essential oils/silver nanoparticles composite films packaging and gamma irradiation on shelf life of strawberries. Food Hydrocolloids, 117, 106750. https://doi.org/10.1016/J.FOODHYD.2021.106750
Sogvar, O. B., Koushesh Saba, M., Emamifar, A., & Hallaj, R. (2016). Influence of nano-ZnO on microbial growth, bioactive content and postharvest quality of strawberries during storage. Innovative Food Science & Emerging Technologies, 35, 168–176. https://doi.org/10.1016/J.IFSET.2016.05.005
Song, X., Wang, L., Liu, T., Liu, Y., Wu, X., & Liu, L. (2021). Mandarin (Citrus reticulata L.) essential oil incorporated into chitosan nanoparticles: Characterization, anti-biofilm properties and application in pork preservation. International Journal of Biological Macromolecules, 185, 620–628. https://doi.org/10.1016/J.IJBIOMAC.2021.06.195
Sullivan, D. J., Cruz-Romero, M., Collins, T., Cummins, E., Kerry, J. P., & Morris, M. A. (2018). Synthesis of monodisperse chitosan nanoparticles. Food Hydrocolloids, 83, 355–364. https://doi.org/10.1016/J.FOODHYD.2018.05.010
Tavassoli, M., Sani, M. A., Khezerlou, A., Ehsani, A., & McClements, D. J. (2021). Multifunctional nanocomposite active packaging materials: Immobilization of quercetin, lactoferrin, and chitosan nanofiber particles in gelatin films. Food Hydrocolloids, 118, 106747. https://doi.org/10.1016/J.FOODHYD.2021.106747
Viacava, G. E., Cenci, M. P., & Ansorena, M. R. (2022). Effect of chitosan edible coatings incorporated with free or microencapsulated thyme essential oil on quality characteristics of fresh-cut carrot slices. Food and Bioprocess Technology, 15(4), 768–784. https://doi.org/10.1007/S11947-022-02783-7
Wang, B., Timilsena, Y. P., Blanch, E., & Adhikari, B. (2017). Mild thermal treatment and in-vitro digestion of three forms of bovine lactoferrin: Effects on functional properties. International Dairy Journal, 64, 22–30. https://doi.org/10.1016/J.IDAIRYJ.2016.09.001
Wang, J., Dou, X., Song, J., Lyu, Y., Zhu, X., Xu, L., Li, W., & Shan, A. (2018). Antimicrobial peptides: Promising alternatives in the post feeding antibiotic era. Medicinal Research Reviews, 39(3), 831–859. https://doi.org/10.1002/med.21542
Wang, M., Chen, L., Liang, Z., He, X., Liu, W., Jiang, B., Yan, J., Sun, P., Cao, Z., Peng, Q., & Lin, Y. E. (2020). Metabolome and transcriptome analyses reveal chlorophyll and anthocyanin metabolism pathway associated with cucumber fruit skin color. BMC Plant Biology, 20(1), 1–13. https://doi.org/10.1186/s12870-020-02597-9
Wang, Y. R., Zhang, B., Fan, J. L., Yang, Q., & Chen, H. Q. (2019). Effects of sodium tripolyphosphate modification on the structural, functional, and rheological properties of rice glutelin. Food Chemistry, 281, 18–27. https://doi.org/10.1016/J.FOODCHEM.2018.12.085
Yang, J., Lu, H., Li, M., Liu, J., Zhang, S., Xiong, L., & Sun, Q. (2017). Development of chitosan-sodium phytate nanoparticles as a potent antibacterial agent. Carbohydrate Polymers, 178, 311–321. https://doi.org/10.1016/J.CARBPOL.2017.09.053
Yang, S., Dai, L., Mao, L., Liu, J., Yuan, F., Li, Z., & Gao, Y. (2019). Effect of sodium tripolyphosphate incorporation on physical, structural, morphological and stability characteristics of zein and gliadin nanoparticles. International Journal of Biological Macromolecules, 136, 653–660. https://doi.org/10.1016/j.ijbiomac.2019.06.052
Zeng, W., Hui, H., Liu, Z., Chang, Z., Wang, M., He, B., & Hao, D. (2021). TPP ionically cross-linked chitosan/PLGA microspheres for the delivery of NGF for peripheral nerve system repair. Carbohydrate Polymers, 258, 117684. https://doi.org/10.1016/J.CARBPOL.2021.117684
Acknowledgements
The authors are grateful for access to the ZetaSizer Nano-ZS equipment from the Biomembrane Laboratory of the Institute of Biology–Unicamp. This research used facilities of the Brazilian Nanotechnology National Laboratory (LNNano), part of the Brazilian Centre for Research in Energy and Materials (CNPEM), a private nonprofit organization under the supervision of the Brazilian Ministry for Science, Technology, and Innovations (MCTI). The staff is acknowledged for assistance during the experiments (TEM 27381).
Funding
This study was supported by National Council for Scientific and Technological Development–CNPq, Brazil (#140320/2017–2, #142480/2020–7), Coordination for the Improvement of Higher Education Personnel–CAPES, Brazil (#001), and São Paulo Research Foundation–FAPESP, Brazil (#2015/26359–0).
Author information
Authors and Affiliations
Contributions
Larissa G. R. Duarte: Investigation; formal analysis; writing, original draft; data curation; Visualization; methodology; validation. Natália C.A. Ferreira: Investigation. Ana Clara T. Fiocco: Formal analysis, Investigation. Carolina S. F. Picone: Conceptualization; resources; supervision; writing, review and editing; project administration; funding acquisition.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Duarte, L.G.R., Ferreira, N.C.A., Fiocco, A.C.T.R. et al. Lactoferrin-Chitosan-TPP Nanoparticles: Antibacterial Action and Extension of Strawberry Shelf-Life. Food Bioprocess Technol 16, 135–148 (2023). https://doi.org/10.1007/s11947-022-02927-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11947-022-02927-9