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ORIGINAL ARTICLE
Sinigrin Encapsulation in Liposomes: Influence on In Vitro Digestion and Antioxidant Potential
| 1 | Institute for Medical Research, University of Belgrade, Dr Subotića 4, 11000 Belgrade, Serbia |
| 2 | Faculty of Chemistry and Technology, University of Split, Ruđera Boškovića 35, 21000 Split, Croatia |
| 3 | Faculty of Science, University of Split, Ruđera Boškovića 33, 21000 Split, Croatia |
| 4 | Division of Gastroenterology and Hepatology, University Hospital Split, Spinčićeva 1, 21000 Split, Croatia |
| 5 | Faculty of Technology and Metallurgy, University of Belgrade, Karnegijeva 4, 11000 Belgrade, Serbia |
CORRESPONDING AUTHOR
Tea Bilusic
Food Technology, University of Split, Faculty of Chemisty and Technology, R.- Boskovica, 21000, Split, Croatia
Food Technology, University of Split, Faculty of Chemisty and Technology, R.- Boskovica, 21000, Split, Croatia
Submission date: 2021-06-21
Final revision date: 2021-11-01
Acceptance date: 2021-11-03
Online publication date: 2021-11-26
Publication date: 2021-11-26
Pol. J. Food Nutr. Sci. 2021;71(4):441–449
KEYWORDS
TOPICS
Liquid chromatographyFunctional foodsMicroencapsulationDigestionFood bioactivesNutraceuticalsVegetables
ABSTRACT
Encapsulation of sinigrin in liposomes with the proliposomal method was performed in order to evaluate the effect of this process on in vitro simulated digestion and antioxidant potential of sinigrin. The recovery of sinigrin after simulated gastric and duodenal digestion of its free and liposomal forms was determined with HPLC-UV using human digestive juices. The antioxidant potential of sinigrin and sinigrin-loaded liposomes was determined with the Rancimat test as their ability to prolong oxidative stability of edible oil. The efficiency of 62% was obtained by encapsulating sinigrin in liposomes. The values of mean diameter, polydispersity index and zeta potential showed satisfactory size uniformity and physical stability of the liposomes containing sinigrin. Liposomes were shown to inhibit the digestion of sinigrin in both human gastric and intestinal juices, clearly enabling its prolonged release. Moreover, sinigrin in the liposomal form significantly prolonged the induction time of edible oil oxidation compared to its free form. The results obtained are encouraging from the point of view of a possible incorporation of the sinigrin-loaded liposomes in real functional food systems or their use as nutraceuticals.
FUNDING
The research was funded by the Croatian Science Foundation within the project “Plants as a source of bioactive sulphur compounds and their ability to hyperracumulate metals” (IP-06-2016-1316).
REFERENCES (55)
1.
Aarak, K.E., Kirkhus, B., Holm, H., Vogt, G., Jacobsen, M., Vegarud, G.E. (2013). Release of EPA and DHA from salmon oil – a comparison of in vitro digestion with human and porcine gastrointestinal enzymes. British Journal of Nutrition, 110(8), 1402-1410. https://doi.org/10.1017/S00071....
2.
Akgün, D., Gültekin-Özgüven, M., Yücetepe, A., Altin, G., Gibis, M., Weiss, J., Özçelik, B. (2020). Stirred-type yoghurt incorporated with sour cherry extract in chitosan-coated liposomes. Food Hydrocolloids, 101, art. no. 105532. https://doi.org/10.1016/j.food....
3.
Almaas, H., Cases, A.L., Devold, T.G., Holm, H., Langsrud, T., Aabakken, L., Aadnoey, T., Vegarud, G.E. (2006). In vitro digestion of bovine and caprine milk by human gastric and duodenal enzymes. International Dairy Journal, 16(9), 961-968. https://doi.org/10.1016/j.idai....
4.
Balanč, B., Trifković, K., Đorđević, V., Marković, S., Pjanović, R., Nedović, V., Bugarski, B. (2016). Novel resveratrol delivery systems based on alginate-sucrose and alginate-chitosan microbeads containing liposomes. Food Hydrocolloids, 61, 832–842. https://doi.org/10.1016/j.food....
5.
Blažević, I., Đulović, A., Maravić, A., Čikeš Čulić, V., Montaut, S., Rollin, P. (2019). Antimicrobial and cytotoxic activities of Lepidium latifolium L. hydrodistillate, extract and its major sulfur volatile allyl isothiocyanate. Chemistry & Biodiversity, 16(4), art. no. e1800661. https://doi.org/10.1002/cbdv.2....
6.
Blažević, I., Montaut, S., Burčul, F., Olsen, C.E., Burow, M., Rollin, P., Agerbirk, N. (2020). Glucosinolate structural diversity, identification, chemical synthesis and metabolism in plants. Phytochemistry, 169, art. no. 112100. https://doi.org/10.1016/j.phyt....
7.
Chen, Y., Wu, Q., Zhang, Z., Yuan, L., Liu, X., Zhou, L. (2012). Preparation of curcumin-loaded liposomes and evaluation of their skin permeation and pharmacodynamics. Molecules, 17(5), 5972-5987. https://doi.org/10.3390/molecu....
8.
Cheng, D.L., Hasimoto, K., Uda, Y. (2004). In vitro digestion of sinigrin and glucotropaeolin by single strains of Bifidobacterium and identification of the digestive products. Food Chemistry and Toxicology, 42(3), 351-357. https://doi.org/10.1016/j.fct.....
9.
Corrales, M., Fernandez, A., Han, J.H. (2014). Antimicrobial packaging systems. Chapter 7, in J.H. Han (Ed.), Innovation in Food Packaging, Elsevier, pp. 133-170. https://doi.org/10.1016/B978-0....
10.
Detoni, C.B., de Oliveira, D.M., Santo, I.E., Pedro, A.S., El-Bacha, R., da Silva Velozo, E., Ferreira, D., Sarmento, B., de Magalhães Cabral-Albuquerque, E.C. (2012). Evaluation of thermal-oxidative stability and antiglioma activity of zanthoxylum tingoassuiba essential oil entrapped into multi- and unilamellar liposomes. Journal of Liposome Research, 22(1), 1-7. https://doi.org/10.3109/089821....
11.
Đorđević, V., Balanč, B., Belščak-Cvitanović, A., Lević, S., Trifković, K., Kalušević, A., Kostić, I., Komes, D., Bugarski, B., Nedović, V. (2015). Trends in encapsulation technologies for delivery of food bioactive compounds. Food Engineering Review, 7, 452-490. https://doi.org/10.1007/s12393....
12.
Emami, S., Azadmard-Damirchi, S., Peighambardoust, S.H., Valizadeh, H., Hesari, J. (2016). Liposomes as carrier vehicles for functional compounds in food sector. Journal of Experimental Nanoscience, 11(9), 737-759. https://doi.org/10.1080/174580....
13.
Ettlinger, M.G., Lundeen, A.J. (1956). The mustard oil of Limnanthes douglasii seed, m-methoxybenzyl isothiocyanate. Journal of American Chemical Society, 78(9), 1952-1954. https://doi.org/10.1021/ja0159....
14.
Furlund, C.B., Ulleberg, E.K., Devold, T.G., Flengsrud, R., Jacobson, M., Sekse, C., Holm, H., Vegarud, G.E. (2013). Identification of lactoferrin peptides generated by digestion with human gastrointestinal enzymes. Journal of Dairy Sciences, 96(1), 75-88. https://doi.org/10.3168/jds.20....
15.
Gaede, H.C., Gawrisch, K. (2003). Lateral diffusion rates of lipid, water, and a hydrophobic drug in a multilamellar liposome. Biophysical Journal, 85(3), 1734-1740. https://doi.org/10.1016/S0006-....
16.
Girgin, N., Nehir El, S. (2015). Effects of cooking on in vitro sinigrin bioaccessibility, total phenols, antioxidant and antimutagenic activity of cauliflower. Journal of Food Composition and Analysis, 37, 119-127. https://doi.org/10.1016/j.jfca....
17.
Gortzi, O., Lalas, S., Tsaknis, J., Chinou, I. (2007). Enhanced bioactivity of Citrus limon (Lemon Greek cultivar) extracts, essential oil and isolated compounds before and after encapsulation in liposomes. Planta Medica, 73, 184. https://doi.org/10.1055/s-2007....
18.
Gortzi, O., Lalas, S., Chinou, I., Tsaknis, J. (2008). Reevaluation of bioactivity and antioxidant activity of Myrtus communis extract before and after encapsulation in liposomes. European Food Research and Technology, 226, 583-590. https://doi.org/10.1007/s00217....
19.
Huang, M., Liang, C., Tan, C, Huang, S., Ying, R., Wang, Y., Zhang, Y. (2019). Liposome co-encapsulation as a strategy for the delivery of curcumin and resveratrol. Food & Function, 10, 6447-6458. https://doi.org/10.1039/C9FO01....
20.
Hwang, E.S., Bornhorst, G.M., Oteiza, P.I., Mitchell, A.E. (2019). Assessing the fate and bioavailability of glucosinolates in kale (Brassica oleracea) using simulated human digestion and Caco-2 cell uptake models. Journal of Agricultural and Food Chemistry, 67(34), 9492-9500. https://doi.org/10.1021/acs.ja....
21.
Isailović, B.D., Kostić, I.T., Zvonar, A., Đorđević, V.B., Gašperlin, M., Nedović, V.A., Bugarski, B.M. (2013). Resveratrol loaded lipsomes produced by different techniques. Innovative Food Science and Emerging Technologies, 19, 181-189. https://doi.org/10.1016/j.ifse....
22.
ISO 6886:1996. Animal and vegetable fats and oil – Determination of oxidation stability (Accelerated oxidation test).
23.
Jie, M., Cheung, W.M., Yu, V., Zhou, Y., Tong, P.H., Ho, J.W.S. (2014). Anti-proliferative activities of sinigrin on carcinogen-induced hepatotoxicity in rats. PLoS ONE, 9(10), art. no. e110145. https://doi.org/10.1371/journa....
24.
Kuljarachanan, T., Fu, N., Chiewchan, N., Devahastin, S., Chen, X.D. (2020). Evolution of important glucosinolates in three common Brassica vegetables during their processing into vegetable powder and in vitro gastric digestion. Food & Function, 11(1), 211-220. https://doi.org/10.1039/C9FO00....
25.
Li, Z., Paulson, A.T., Gil, T.A. (2015). Encapsulation of bioactive salmon protein hydrolysates with chitosan-coated lipsomes. Journal of Functional Foods, 19, Part A, 733-743. https://doi.org/10.1016/j.jff.....
26.
Lin, L., Zhu, Y., Thangaraj, B., Abdel-Samie, M.A.S., Cui, H. (2018). Improving the stability of thyme essential oil solid liposome by using β-cyclodextrin as a cryoprotectant. Carbohydrate Polymers, 188, 243–251. https://doi.org/10.1016/j.carb....
27.
Liović, N., Bošković, P., Drvenica, I., Režek Jambrak, A., Dropulić, A.M., Krešić, G., Nedović, V., Zorić, Z., Pedisić, S., Bilušić, T. (2019). Phenolic extracts from Vaccinium corymbosum L. loaded in microemulsions and liposomes as enhancers of olive oil oxidative stability. Polish Journal of Food Nutrition and Sciences, 69(1), 23-33. https://doi.org/10.31883/pjfns....
28.
Liu, W., Ye, Y., Han, F., Han, J. (2019). Advances and challenges in liposome digestion: Surface interaction, biological fate, and GIT modeling. Advances in Colloid and Interface Science, 263, 52-67. https://doi.org/10.1016/j.cis.....
29.
Liu, W., Hou, Y., Jin, Y., Wang, Y., Xu, X., Han, J. (2020). Research progress on liposomes: Application in food, digestion behavior and absorption mechanism. Trends in Food Science & Technology, 104, 177–189. https://doi.org/10.1016/j.tifs....
30.
Malheiros, P.S., Daroit, D.J., Brandelli, A. (2010). Food applications of liposome encapsulated antimicrobial peptides. Trends in Food Science & Technology, 21(6), 284-292. https://doi.org/10.1016/j.tifs....
31.
Maruthupandy, M., Seo, J. (2019). Allyl isothiocyanate encapsulated halloysite covered with polyacrylate as a potential antibacterial agent against food spoilage bacteria. Materials Science and Enginerring: C, Material for Biological Application, 105, art. no. 110016. https://doi.org/10.1016/j.msec....
32.
Mateos, H., Valentini, A., Robles, E., Brooker, A., Cioffi, N., Palazzo, G. (2019). Measurement of the zeta-potential of solid surfaces through Laser Doppler Electrophoresis of colloid tracer in a dip-cell: survey of the effect of ionic strength, pH, tracer chemical nature and size. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 576, 82–90. https://doi.org/10.1016/j.cols....
33.
Mazumder, A., Dwivedi, A., Fox, L.T., Brümer, A., du Preez, J., Gerber, M., du Plessis, J. (2016). In vitro skin permeation of sinigrin from its phytosome complex. Journal of Pharmacy and Pharmacology, 68(12), 1577-1583. https://doi.org/10.1111/jphp.1....
34.
Melrose, J. (2019). The glucosinolates: A sulphur glucoside family of mustard anti-tumor and antimicrobial phytochemicals of potential therapeutic application. Biomedicines, 7(3), art. no. 62. https://doi.org/10.3390/biomed....
35.
Mithen, R., Bennet, R., Marquez, J. (2010). Glucosinolate biochemical diversity and innovation in the Brassicales. Phytochemistry, 71(17-18), 2074-2086. https://doi.org/10.1016/j.phyt....
36.
Mitsiogianni, M., Koutsidis, G., Mavroudis, N., Trafalis, D. T., Botaitis, S., Franco, R., Zoumpourlis, V., Amery, T., Galanis, A., Pappa, A., Panayiotidis, M.I. (2019). The role of isothiocyanates as cancer chemo-preventive, chemo-therapeutic and anti-melanoma agents. Antioxidants, 8(4), art. no. 106. https://doi.org/10.3390/antiox....
37.
Moghimipour, E., Aghel, N., Mahmoudabadi, A.Z., Ramezani, Z., Handali, S. (2012), Preparation and characterization of liposomes containing essential oil of Eucalyptus camaldulensis leaf. Junidshapur Journal of Natural Pharmaceutical Products, 7(3), 117-122. https://doi.org/10.17795/jjnpp....
38.
Park, S.Y., Barton, M., Pendleton, P. (2012). Controlled release of allyl isothiocyanate for bacteria growth management. Food Control, 23(2), 478-484. https://doi.org/10.1016/j.food....
39.
Pinilla, C.M.B., Noreña, C.P.Z., Brandelli, A. (2017). Development and characterization of phosphatidylcholine nanovesicles, containing garlic extract, with antilisterial activity in milk. Food Chemistry, 220, 470-76. https://doi.org/10.1016/j.food....
40.
Pothakamury, U.R., Barbosa-C‘anovas, G.V. (1995). Fundamental aspects of controlled release in foods. Trends in Food Science & Technology, 6(12), 397–406. https://doi.org/10.1016/S0924-....
41.
Pulliero, A., Wu, Y., Fenoglio, D., Parodi, A., Romani, M., Soares, C.P., Filaci, G., Lee, J.L., Sinkam, P.N., Izzotti, A. (2015). Nanoparticles increase the efficacy of cancer chemopreventive agents in cells exposed to cigarette smoke condensate. Carcinogenesis, 36(3), 368-377. https://doi.org/10.1093/carcin....
42.
Radünz, M., Dos Santos Hackbart, H.C., Pontes Bona, N., Stark Pedra, N., Hoffman, J.F., Moro Stefanello, F., Da Rosa Zavareze, E. (2020). Glucosinolates and phenolic compounds rich broccoli extract: Encapsulation by electrospraying and antitumor activity against glial tumor cells. Colloids and Surfaces B: Biointerfaces, 192, art. no. 111020. https://doi.org/10.1016/j.cols....
43.
Rashidinejad, A., Birch, E.J., Sun-Waterhouse, D., Everett, D.W. (2014). Delivery of green tea catechin and epigallocatechin gallate in liposomes incorporated into low-fat hard cheese. Food Chemistry, 156, 176-183. https://doi.org/10.1016/j.food....
44.
Romeo, L., Iori, R., Rollin, P., Bramanti, P., Mazzon, E. (2018). Isothiocyanates: An overview of their antimicrobial activity against human infections. Molecules, 23(3), art. no. 624. https://doi.org/10.3390/molecu....
45.
Savaghebi, D., Barzegar, M., Mozafari, M.R. (2020). Manufacturing of nanoliposomal extract from Sargassum boveanum algae and investigating its release behavior and antioxidant activity. Food Science & Nutrition, 8(1), 299–310. https://doi.org/10.1002/fsn3.1....
46.
Sun, M., Dang, U.J., Di Pasqua, A.J. (2019). Phenethyl isothiocyanate and cisplatin co-encapsulated in a liposomal nanoparticle for treatment of non-small cell lung cancer. Molecules, 24(4), art. no. 801. https://doi.org/10.3390/molecu....
47.
Takahashi, M., Uechi, S., Takara, K., Asikin, Y., Wada, K. (2009). Evaluation of an oral carrier system in rats: bioavailability and antioxidant properties of liposome-encapsulated curcumin. Journal of Agricultural and Food Chemistry, 57(19), 9141-9146. https://doi.org/10.1021/jf9013....
48.
Tsao, R., Yu, Q., Friesen, I., Potter, J., Chiba, M. (2000). Factors affecting the dissolution and degradation of oriental mustard-derived sinigrin and allyl isothiocyanate in aqueous media. Journal of Agricultural Food Chemistry, 48(5), 1898-1902. https://doi.org/10.1021/jf9906....
49.
Waser, L.R., Watson, W.H. (1963). Crystal structure of sinigrin. Nature, 198, 1297-1298. https://doi.org/10.1038/198129....
50.
Wechtersbach, L., Poklar Ulrih, N., Cigic, B. (2012). Liposomal stabilization of ascorbic acid in model systems and in food matrices. LWT – Food Science and Technology, 45(1), 43-49. https://doi.org/10.1016/j.lwt.....
51.
Weil, M.J., Zhang, Y., Nair, M.G. (2004). Colon cancer proliferating desulfosinigrin in wasabi (Wasabia japonica). Nutrition and Cancer, 48(2), 207-213. https://doi.org/10.1207/s15327....
52.
Wu, X., Zhou, Q., Xu, K. (2009). Are isothiocyanates potential anti-cancer drugs? Acta Pharmacologica Sinica, 30, 501-512. https://doi.org/10.1038/aps.20....
53.
Zorić, Z., Markić, J., Pedisić, S., Bučević-Popović, V., Generalić-Mekinić, I., Grebenar, K., Bilušić, T. (2016). Stability of rosmarinic acid in aqueous extracts from different Lamiaceae species after in vitro digestion with human gastrointestinal enzymes. Food Technology and Biotechnology, 54(1), 97-102. https://doi.org/10.17113/ftb.5....
54.
Yang, S., Liu, W., Liu, C., Liu, W., Tong, G., Zheng, H., Zhou, W. (2012). Characterization and bioavailability of vitamin C nanoliposomes prepared by film evaporation-dynamic high pressure microfluidization. Journal of Dispersion Science and Technology, 33(11), 1608-1614. https://doi.org/10.1080/019326....
55.
Yuan, Y.G., Zhang, S., Hwang, J.Y., Kong, I.K. (2018). Nanoparticles potentiates cytotoxicity and apoptotic potential of camptothecin in human cervical cancer cells. Oxidative Medicine and Cellular Longevity, 2018, art. no. 6121328. https://doi.org/10.1155/2018/6....
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