Abstract
Curcumin solid lipid nanoparticles were prepared by microemulsion method, and the physicochemical properties of these products were characterized. High encapsulation efficiency and good stability were presented (encapsulation efficiency: 89.86%, drug load rate: 28.63%, particle size: 291 ± 5.34 nm, zeta potential: − 44.4 ± 0.46 mV, stability time: > 4 weeks). The antibacterial experiments through photodynamic inactivation against two food-related microorganisms were carried out in carrot juice. The results demonstrated that the inactivation efficiency of photodynamic inactivation mediated by curcumin solid lipid nanoparticles was greater than that of free curcumin, and more stable in preserved quality at that. Moreover, the microbiota in photodynamic inactivation mediated by curcumin solid lipid nanoparticles group was kept below limit of detection for 28 days of storage while viable microorganisms were detected in free curcumin group. This study identified that photodynamic inactivation mediated by curcumin solid lipid nanoparticles could meet the requirements of food sterilization and produce safe carrot juice with preserved quality attributes.
Similar content being viewed by others
Data Availability
Due to the nature of this research, participants of this study did not agree for their data to be shared publicly, so supporting data is not available.
References
Abarca, R. L., Rodríguez, F. J., Guarda, A., Galotto, M. J., & Bruna, J. E. (2016). Characterization of beta-cyclodextrin inclusion complexes containing an essential oil component. Food Chemistry, 196, 968–975.
Abdulrahman, H., Misba, L., Ahmad, S., & Khan, A. U. (2020). Curcumin induced photodynamic therapy mediated suppression of quorum sensing pathway of Pseudomonas aeruginosa: An approach to inhibit biofilm in vitro. Photodiagnosis and Photodynamic Therapy, 30, 101645.
Alklint, C., Wadsö, L., & Sjöholm, I. (2004). Effects of modified atmosphere on shelf-life of carrot juice. Food Control, 15(2), 131–137.
Baykuş, G., Akgün, M. P., & Unluturk, S. (2021). Effects of ultraviolet-light emitting diodes (UV-LEDs) on microbial inactivation and quality attributes of mixed beverage made from blend of carrot, carob, ginger, grape and lemon juice. Innovative Food Science & Emerging Technologies, 67, 102572.
Bhavya, M. L., & Hebbar, H. U. (2019). Sono-photodynamic inactivation of Escherichia coli and Staphylococcus aureus in orange juice. Ultrasonics Sonochemistry, 57, 108–115.
Bhavya, M. L., Shewale, S. R., Rajoriya, D., & Hebbar, H. U. (2021). Impact of blue LED illumination and natural photosensitizer on bacterial pathogens, enzyme activity and quality attributes of fresh-cut pineapple slices. Food and Bioprocess Technology, 14(2), 362–372.
Bi, X., Zhou, Z., Wang, X., Jiang, X., Chen, L., Xing, Y., & Che, Z. (2020). Changes in the microbial content and quality attributes of carrot juice treated by a combination of ultrasound and Nisin during storage. Food and Bioprocess Technology, 13(9), 1556–1565.
Bialka, K. L., & Demirci, A. (2008). Efficacy of pulsed UV-light for the decontamination of Escherichia coli O157:H7 and Salmonella spp. on raspberries and strawberries. Journal Food of Science, 73(5), M201–207.
Caminiti, I. M., Palgan, I., Muñoz, A., Noci, F., Whyte, P., Morgan, D. J., Cronin, D. A., & Lyng, J. G. (2012). The effect of ultraviolet light on microbial inactivation and quality attributes of apple juice. Food and Bioprocess Technology, 5(2), 680–686.
Chen, L., Bi, X., Guo, D., Xing, Y., & Che, Z. (2019). The effect of high-power ultrasound on the quality of carrot juice. Food Science and Technology International, 25(5), 394–403.
Cheng, J.-H., Lv, X., Pan, Y., & Sun, D.-W. (2020). Foodborne bacterial stress responses to exogenous reactive oxygen species (ROS) induced by cold plasma treatments. Trends in Food Science & Technology, 103, 239–247.
Ciancaglini, P., Santos, H. L., Daghastanli, K. R. P., & Thedei, G. (2001). Using a classical method of vitamin C quantification as a tool for discussion of its role in the body. Biochemistry and Molecular Biology Education, 29(3), 110–114.
Cieplik, F., Deng, D., Crielaard, W., Buchalla, W., Hellwig, E., Al-Ahmad, A., & Maisch, T. (2018). Antimicrobial photodynamic therapy - what we know and what we don’t. Critical Reviews in Microbiology, 44(5), 571–589.
de Ancos, B., Sgroppo, S., Plaza, L., & Cano, M. P. (2002). Possible nutritional and health-related value promotion in orange juice preserved by high-pressure treatment. Journal of the Science of Food and Agriculture, 82(8), 790–796.
de Andrade Neto, J. B., de Farias Cabral, V. P., Nogueira, L. F. B., da Silva, C. R., Sá, L. G., da Silva A. R., da Silva, W. M., Silva, J., Marinho, E. S., Cavalcanti, B. C., de Moraes M. O., & Nobre Júnior, H. V. (2021). Anti-MRSA activity of curcumin in planktonic cells and biofilms and determination of possible action mechanisms. Microbial Pathogenesis, 155, 104892.
Dede, S., Alpas, H., & Bayındırlı, A. (2007). High hydrostatic pressure treatment and storage of carrot and tomato juices: Antioxidant activity and microbial safety. Journal of the Science of Food and Agriculture, 87(5), 773–782.
de Oliveira, E. F., Tikekar, R., & Nitin, N. (2018). Combination of aerosolized curcumin and UV-A light for the inactivation of bacteria on fresh produce surfaces. Food Research International, 114, 133–139.
de Paula Ribeiro, I., Pinto, J. G., Souza, B. M. N., Miñán, A. G., & Ferreira-Strixino, J. (2022). Antimicrobial photodynamic therapy with curcumin on methicillin-resistant Staphylococcus aureus biofilm. Photodiagnosis and Photodynamic Therapy, 37, 102729.
Derradji-Benmeziane, F., Djamai, R., & Cadot, Y. (2014). Antioxidant capacity, total phenolic, carotenoid, and vitamin C contents of five table grape varieties from Algeria and their correlations. OENO One, 48(2), 153–162.
Dias, L. D., Blanco, K. C., Mfouo-Tynga, I. S., Inada, N. M., & Bagnato, V. S. (2020). Curcumin as a photosensitizer: From molecular structure to recent advances in antimicrobial photodynamic therapy. Journal of Photochemistry and Photobiology C: Photochemistry Reviews, 45, 100384.
Dolatabadi, S., Karimi, M., Nasirizadeh, S., Hatamipour, M., Golmohammadzadeh, S., & Jaafari, M. R. (2021). Preparation, characterization and in vivo pharmacokinetic evaluation of curcuminoids-loaded solid lipid nanoparticles (SLNs) and nanostructured lipid carriers (NLCs). Journal of Drug Delivery Science and Technology, 62, 102352.
Farkas, D. F., & Hoover, D. G. (2000). High pressure processing. Journal of Food Science, 65(s8), 47–64.
Farnworth, E. R., Lagacé, M., Couture, R., Yaylayan, V., & Stewart, B. (2001). Thermal processing, storage conditions, and the composition and physical properties of orange juice. Food Research International, 34(1), 25–30.
Fathi, M., Varshosaz, J., Mohebbi, M., & Shahidi, F. (2013). Hesperetin-loaded solid lipid nanoparticles and nanostructure lipid carriers for food fortification: Preparation, characterization, and modeling. Food and Bioprocess Technology, 6(6), 1464–1475.
García Carrillo, M., Ferrario, M., Schenk, M., & Guerrero, S. (2020). Effect of an UV-C light-based hurdle strategy for carrot-orange juice processing on Candida parapsilosis inactivation and physiological state: Impact on juice sensory and physicochemical quality parameters. Food and Bioprocess Technology, 13(11), 1954–1967.
Gayán, E., Condón, S., & Álvarez, I. (2014). Biological aspects in food preservation by ultraviolet light: A REVIEW. Food and Bioprocess Technology, 7(1), 1–20.
Ghate, V. S., Ng, K. S., Zhou, W., Yang, H., Khoo, G. H., Yoon, W.-B., & Yuk, H.-G. (2013). Antibacterial effect of light emitting diodes of visible wavelengths on selected foodborne pathogens at different illumination temperatures. International Journal of Food Microbiology, 166(3), 399–406.
Gouma, M., Álvarez, I., Condón, S., & Gayán, E. (2020). Pasteurization of carrot juice by combining UV-C and mild heat: Impact on shelf-life and quality compared to conventional thermal treatment. Innovative Food Science & Emerging Technologies, 64, 102362.
Gu, W., Liu, D., & Sun, J. (2022). Co-crystallization of curcumin for improved photodynamic inactivation of Vibrio parahaemolyticus and its application for the preservation of cooked clams. International Journal of Food Microbiology, 378, 109816.
Haukvik, T., Bruzell, E., Kristensen, S., & Tønnesen, H. H. (2009). Photokilling of bacteria by curcumin in different aqueous preparations. Studies on curcumin and curcuminoids XXXVII. Pharmazie, 64(10), 666–673.
Huang, J., Chen, B., Zeng, Q.-H., Liu, Y., Liu, H., Zhao, Y., & Wang, J. J. (2021). Application of the curcumin-mediated photodynamic inactivation for preserving the storage quality of salmon contaminated with L. monocytogenes. Food Chemistry, 359, 129974.
Jori, G., Fabris, C., Soncin, M., Ferro, S., Coppellotti, O., Dei, D., Fantetti, L., Chiti, G., & Roncucci, G. (2006). Photodynamic therapy in the treatment of microbial infections: Basic principles and perspective applications. Lasers in Surgery and Medicine, 38(5), 468–481.
Kaur, S., Modi, N. H., Panda, D., & Roy, N. (2010). Probing the binding site of curcumin in Escherichia coli and Bacillus subtilis FtsZ – A structural insight to unveil antibacterial activity of curcumin. European Journal of Medicinal Chemistry, 45(9), 4209–4214.
Kwiatkowski, S., Knap, B., Przystupski, D., Saczko, J., Kędzierska, E., Knap-Czop, K., Kotlińska, J., Michel, O., Kotowski, K., & Kulbacka, J. (2018). Photodynamic therapy – Mechanisms, photosensitizers and combinations. Biomedicine & Pharmacotherapy, 106, 1098–1107.
Lai, D., Zhou, A., Tan, B. K., Tang, Y., Sarah Hamzah, S., Zhang, Z., Lin, S., & Hu, J. (2021). Preparation and photodynamic bactericidal effects of curcumin-β-cyclodextrin complex. Food Chemistry, 361, 130117.
Lee, I.-H., Cho, E.-R., & Kang, D.-H. (2023). The effect of quercetin mediated photodynamic inactivation on apple juice properties at different temperature and its bactericidal mechanism. Food Control, 144, 109362.
Martínez-Hernández, G. B., Álvarez-Hernández, M. H., & Artés-Hernández, F. (2019). Browning control using cyclodextrins in high pressure–treated apple juice. Food and Bioprocess Technology, 12(4), 694–703.
Mei, L., Zhang, Z., Zhao, L., Huang, L., Yang, X.-L., Tang, J., & Feng, S.-S. (2013). Pharmaceutical nanotechnology for oral delivery of anticancer drugs. Advanced Drug Delivery Reviews, 65(6), 880–890.
Nadeem, M., Ubaid, N., Qureshi, T. M., Munir, M., & Mehmood, A. (2018). Effect of ultrasound and chemical treatment on total phenol, flavonoids and antioxidant properties on carrot-grape juice blend during storage. Ultrasonics Sonochemistry, 45, 1–6.
Nardo, L., Paderno, R., Andreoni, A., Másson, M., Haukvik, T., & Tønnesen, H. H. (2008). Role of H-bond formation in the photoreactivity of curcumin. Spectroscopy, 22, 187–198.
Odriozola-Serrano, I., Soliva-Fortuny, R., & Martín-Belloso, O. (2008). Changes of health-related compounds throughout cold storage of tomato juice stabilized by thermal or high intensity pulsed electric field treatments. Innovative Food Science & Emerging Technologies, 9(3), 272–279.
Pan, Y., Sun, D.-W., & Han, Z. (2017). Applications of electromagnetic fields for nonthermal inactivation of microorganisms in foods: An overview. Trends in Food Science & Technology, 64, 13–22.
Pardeike, J., Hommoss, A., & Müller, R. H. (2009). Lipid nanoparticles (SLN, NLC) in cosmetic and pharmaceutical dermal products. International Journal of Pharmaceutics, 366(1), 170–184.
Penha, C. B., Bonin, E., da Silva, A. F., Hioka, N., Zanqueta, É. B., Nakamura, T. U., de Abreu Filho, B. A., Campanerut-Sá, P. A. Z., & Mikcha, J. M. G. (2017). Photodynamic inactivation of foodborne and food spoilage bacteria by curcumin. LWT - Food Science and Technology, 76, 198–202.
Pokhrel, P. R., Boulet, C., Yildiz, S., Sablani, S., Tang, J., & Barbosa-Cánovas, G. V. (2022). Effect of high hydrostatic pressure on microbial inactivation and quality changes in carrot-orange juice blends at varying pH. LWT, 159, 113219.
Radi, M., Ahmadi, H., & Amiri, S. (2022). Effect of cinnamon essential oil-loaded nanostructured lipid carriers (NLC) against Penicillium citrinum and Penicillium expansum involved in tangerine decay. Food and Bioprocess Technology, 15(2), 306–318.
Ravanfar, R., Tamaddon, A. M., Niakousari, M., & Moein, M. R. (2016). Preservation of anthocyanins in solid lipid nanoparticles: Optimization of a microemulsion dilution method using the Placket-Burman and Box-Behnken designs. Food Chemistry, 199, 573–580.
Riganakos, K. A., Karabagias, I. K., Gertzou, I., & Stahl, M. (2017). Comparison of UV-C and thermal treatments for the preservation of carrot juice. Innovative Food Science & Emerging Technologies, 42, 165–172.
Sepahvand, S., Amiri, S., Radi, M., & Akhavan, H.-R. (2021). Antimicrobial activity of thymol and thymol-nanoemulsion against three food-borne pathogens inoculated in a sausage model. Food and Bioprocess Technology, 14(10), 1936–1945.
Shao, L., Sun, Y., Zou, B., Zhao, Y., Li, X., & Dai, R. (2023). Sublethally injured microorganisms in food processing and preservation: Quantification, formation, detection, resuscitation and adaption. Food Research International, 165, 112536.
Sheng, L., Li, X., & Wang, L. (2022). Photodynamic inactivation in food systems: A review of its application, mechanisms, and future perspective. Trends in Food Science & Technology, 124, 167–181.
Silva, H. D., Cerqueira, M. A., Donsì, F., Pinheiro, A. C., Ferrari, G., & Vicente, A. A. (2020). Development and characterization of lipid-based nanosystems: Effect of interfacial composition on nanoemulsion behavior. Food and Bioprocess Technology, 13(1), 67–87.
Suwannasang, S., Thumthanaruk, B., Zhong, Q., Uttapap, D., Puttanlek, C., Vatanyoopaisarn, S., & Rungsardthong, V. (2021). The improved properties of zein encapsulating and stabilizing sacha inchi oil by surfactant combination of lecithin and Tween 80. Food and Bioprocess Technology, 14(11), 2078–2090.
Tamjidi, F., Shahedi, M., Varshosaz, J., & Nasirpour, A. (2013). Nanostructured lipid carriers (NLC): A potential delivery system for bioactive food molecules. Innovative Food Science & Emerging Technologies, 19, 29–43.
Tao, R., Zhang, F., Tang, Q.-j, Xu, C.-s, Ni, Z.-J., & Meng, X.-h. (2019). Effects of curcumin-based photodynamic treatment on the storage quality of fresh-cut apples. Food Chemistry, 274, 415–421.
Tenchov, R., Bird, R., Curtze, A. E., & Zhou, Q. (2021). Lipid nanoparticles─From liposomes to mRNA vaccine delivery, a landscape of research diversity and advancement. ACS Nano, 15(11), 16982–17015.
Walkling-Ribeiro, M., Noci, F., Cronin, D. A., Riener, J., Lyng, J. G., & Morgan, D. J. (2008). Reduction of Staphylococcus aureus and quality changes in apple juice processed by ultraviolet irradiation, pre-heating and pulsed electric fields. Journal of Food Engineering, 89(3), 267–273.
Wang, H., Hao, L., Niu, B., Jiang, S., Cheng, J., & Jiang, S. (2016). Kinetics and antioxidant capacity of proanthocyanidins encapsulated in zein electrospun fibers by cyclic voltammetry. Journal of Agricultural and Food Chemistry, 64(15), 3083–3090.
Wang, Y., Liu, F., Cao, X., Chen, F., Hu, X., & Liao, X. (2012). Comparison of high hydrostatic pressure and high temperature short time processing on quality of purple sweet potato nectar. Innovative Food Science & Emerging Technologies, 16, 326–334.
Woodling, S. E., & Moraru, C. I. (2007). Effect of spectral range in surface inactivation of listeria innocua using broad-spectrum pulsed light. Journal of Food Protection, 70(4), 909–916.
Xu, J., Zhou, L., Miao, J., Yu, W., Zou, L., Zhou, W., Liu, C., & Liu, W. (2020). Effect of cinnamon essential oil nanoemulsion combined with ascorbic acid on enzymatic browning of cloudy apple juice. Food and Bioprocess Technology, 13(5), 860–870.
Yang, Q.-Q., Farha, A. K., Kim, G., Gul, K., Gan, R.-Y., & Corke, H. (2020). Antimicrobial and anticancer applications and related mechanisms of curcumin-mediated photodynamic treatments. Trends in Food Science & Technology, 97, 341–354.
Yin, R., Dai, T., Avci, P., Jorge, A. E., de Melo, W. C., Vecchio, D., Huang, Y. Y., Gupta, A., & Hamblin, M. R. (2013). Light based anti-infectives: Ultraviolet C irradiation, photodynamic therapy, blue light, and beyond. Current Opinion in Pharmacology, 13(5), 731–762.
Yoo, S., Ghafoor, K., Kim, J. U., Kim, S., Jung, B., Lee, D.-U., & Park, J. (2015). Inactivation of Escherichia coli O157:H7 on orange fruit surfaces and in juice using photocatalysis and high hydrostatic pressure. Journal of Food Protection, 78(6), 1098–1105.
Yu, J., Zhang, F., Zhang, J., Han, Q., Song, L., & Meng, X. (2021). Effect of photodynamic treatments on quality and antioxidant properties of fresh-cut potatoes. Food Chemistry, 362, 130224.
Zhou, F., Lin, S., Zhang, J., Kong, Z., Tan, B. K., Hamzah, S. S., & Hu, J. (2022). Enhancement of photodynamic bactericidal activity of curcumin against Pseudomonas Aeruginosa using polymyxin B. Photodiagnosis and Photodynamic Therapy, 37, 102677.
Zhu, S., Song, Y., Pei, J., Xue, F., Cui, X., Xiong, X., & Li, C. (2021). The application of photodynamic inactivation to microorganisms in food. Food Chemistry: X, 12, 100150.
Zhu, Y., Li, C., Cui, H., & Lin, L. (2019). Antimicrobial mechanism of pulsed light for the control of Escherichia coli O157:H7 and its application in carrot juice. Food Control, 106, 106751.
Zhu, Z., Cai, H., & Sun, D.-W. (2018). Titanium dioxide (TiO2) photocatalysis technology for nonthermal inactivation of microorganisms in foods. Trends in Food Science & Technology, 75, 23–35.
Funding
This work was supported by the governmental service funds of Ministry of Agriculture and Rural Affairs, PRC (grant number 08200130) and the open project funds of Beijing Laboratory of Food Quality and Safety/Key Laboratory of Alcoholic Beverages Quality and Safety of China Light Industry (grant number FQS-202203).
Author information
Authors and Affiliations
Contributions
Yihang Liu and Suilou Wang contributed equally to this work. Yihang Liu: methodology, sampling, measurement and writing original draft; Suilou Wang: experiment design and supervision; Jiayi Wu: data collection and analysis; Guohong Qi: consulting and data curation; Guitang Chen: data validation; Hehe Li: conceptualization and resources; Haixiang Wang: project administration, supervision, funding acquisition and article revision.
Corresponding authors
Ethics declarations
Competing Interests
The authors declare that there is no conflict of interest.
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
Liu, Y., Wang, S., Wu, J. et al. Photodynamic Inactivation Mediated by Curcumin Solid Lipid Nanoparticles on Bacteria and Its Application for Fresh Carrot Juice. Food Bioprocess Technol 17, 1294–1308 (2024). https://doi.org/10.1007/s11947-023-03199-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11947-023-03199-7