Microencapsulation of Phenolic Extract from Sea Grape (Coccoloba uvifera L.) with Antimutagenic Activity
Montserrat Calderón-Santoyo
Laboratorio Integral de Investigación en Alimentos, Tecnológico Nacional de México/Instituto Tecnológico de Tepic, Tepic, Nayarit, México
Search for more papers by this authorElda Margarita González-Cruz
Departamento de Estudios de Posgrado e Investigación, Tecnológico Nacional de México/Instituto Tecnológico de Tlajomulco, Tlajomulco de Zúñiga, Jalisco, Mexico
Search for more papers by this authorMaricarmen Iñiguez-Moreno
Laboratorio Integral de Investigación en Alimentos, Tecnológico Nacional de México/Instituto Tecnológico de Tepic, Tepic, Nayarit, México
Universidad Politécnica del Estado de Nayarit, Tepic, Nayarit, México
Search for more papers by this authorOsvaldo Ramos-Martínez
Laboratorio Integral de Investigación en Alimentos, Tecnológico Nacional de México/Instituto Tecnológico de Tepic, Tepic, Nayarit, México
Search for more papers by this authorArmando Burgos-Hernández
Departamento de Investigación y Posgrado en Alimentos, Universidad de Sonora, Hermosillo, Sonora, Mexico
Search for more papers by this authorCorresponding Author
Juan Arturo Ragazzo-Sánchez
Laboratorio Integral de Investigación en Alimentos, Tecnológico Nacional de México/Instituto Tecnológico de Tepic, Tepic, Nayarit, México
Search for more papers by this authorMontserrat Calderón-Santoyo
Laboratorio Integral de Investigación en Alimentos, Tecnológico Nacional de México/Instituto Tecnológico de Tepic, Tepic, Nayarit, México
Search for more papers by this authorElda Margarita González-Cruz
Departamento de Estudios de Posgrado e Investigación, Tecnológico Nacional de México/Instituto Tecnológico de Tlajomulco, Tlajomulco de Zúñiga, Jalisco, Mexico
Search for more papers by this authorMaricarmen Iñiguez-Moreno
Laboratorio Integral de Investigación en Alimentos, Tecnológico Nacional de México/Instituto Tecnológico de Tepic, Tepic, Nayarit, México
Universidad Politécnica del Estado de Nayarit, Tepic, Nayarit, México
Search for more papers by this authorOsvaldo Ramos-Martínez
Laboratorio Integral de Investigación en Alimentos, Tecnológico Nacional de México/Instituto Tecnológico de Tepic, Tepic, Nayarit, México
Search for more papers by this authorArmando Burgos-Hernández
Departamento de Investigación y Posgrado en Alimentos, Universidad de Sonora, Hermosillo, Sonora, Mexico
Search for more papers by this authorCorresponding Author
Juan Arturo Ragazzo-Sánchez
Laboratorio Integral de Investigación en Alimentos, Tecnológico Nacional de México/Instituto Tecnológico de Tepic, Tepic, Nayarit, México
Search for more papers by this authorAbstract
This study aimed to microencapsulate the sea grape ethanolic extract by the spray drying process, characterizing the obtained powder, and evaluating its antimutagenicity activity. Microparticles showed a mean size of 6.28 μm and a spherical shape with a smooth surface. The powder had a low moisture content (4.02±0.92 %) and water activity (0.27±0.01), and high solubility (76±3.60 %). Moreover, hygroscopicity (14.75±2.63 g/100 g of powder) and bulk density (0.63±0.03 g/cm3) values suggested that this powder can be easily handled at a pilot or industrial scale. In addition, microencapsulation protected the extract against oxidation by ultraviolet light, improved its thermal stability, and its antimutagenicity activity was similar to fresh sea grape extract. In conclusion, the microencapsulation with maltodextrin by spray drying technique is an alternative to protect bioactive compounds from sea grapes against environmental conditions, maintaining their antimutagenic activity.
Graphical Abstract
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Open Research
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
- 1S. Kim, Y. Shon, J. Lee, C. Kim, K. Nam, ‘Antimutagenic activity of soybeans fermented with basidiomycetes in Ames/Salmonella test’, Biotechnol. Lett. 2000, 22, 1197–1202.
- 2G. Ruiz-Montañez, J. A. Ragazzo-Sanchez, L. Picart-Palmade, M. Calderón-Santoyo, D. Chevalier-Lucia, ‘Optimization of nanoemulsions processed by high-pressure homogenization to protect a bioactive extract of jackfruit (Artocarpus heterophyllus Lam)’, Innovative Food Sci. Emerging Technol. 2017, 40, 35–41.
- 3S. Ramos-Bell, M. Calderón-Santoyo, J. C. Barros-Castillo, J. A. Ragazzo-Sánchez, ‘Characterization of submicron emulsion processed by ultrasound homogenization to protect a bioactive extract from sea grape (Coccoloba uvifera L.)’, Food Sci. Biotechnol. 2020, 10, 1365–1372.
- 4M. R. Segura Campos, J. Ruiz Ruiz, L. Chel-Guerrero, D. Betancur Ancona, ‘Coccoloba uvifera (L.) (Polygonaceae) fruit: Phytochemical screening and potential antioxidant activity’, J. Chem. 2015, 2015.
- 5L. Zhao, F. Temelli, L. Chen, ‘Encapsulation of anthocyanin in liposomes using supercritical carbon dioxide: Effects of anthocyanin and sterol concentrations’, J. Funct. Foods 2017, 34, 159–167.
- 6L. Lee, I. T. Norton, ‘Comparing droplet breakup for a high-pressure valve homogeniser and a Microfluidizer for the potential production of food-grade nanoemulsions’, J. Food Eng. 2013.
- 7P. M. C. L. Reis, N. Mezzomo, G. P. S. Aguiar, E. M. T. L. Senna, H. Hense, S. R. S. Ferreira, ‘Ultrasound-assisted emulsion of laurel leaves essential oil (Laurus nobilis L.) encapsulated by SFEE’, J. Supercrit. Fluids 2019, 147, 284–292.
- 8G. Ruiz-Montañez, M. Calderón-Santoyo, D. Chevalier-Lucia, L. Picart-Palmade, D. E. Jimenez-Sánchez, J. A. Ragazzo-Sánchez, ‘Ultrasound-assisted microencapsulation of jackfruit extract in eco-friendly powder particles: characterization and antiproliferative activity’, J. Dispersion Sci. Technol. 2019, 40, 1507–1515.
- 9A. Madene, M. Jacquot, J. Scher, S. Desobry, ‘Flavour encapsulation and controlled release - A review’, Int. J. Food Sci. Technol. 2006, 41, 1–21.
- 10E. C. Frascareli, V. M. Silva, R. V. Tonon, M. D. Hubinger, ‘Effect of process conditions on the microencapsulation of coffee oil by spray drying’, Food Bioprod. Process. 2012, 90, 413–424.
- 11P. Melin, I. Sundh, S. Håkansson, J. Schnürer, ‘Biological preservation of plant derived animal feed with antifungal microorganisms: Safety and formulation aspects’, Biotechnol. Lett. 2007, 29, 1147–1154.
- 12L. F. Ballesteros, M. J. Ramirez, C. E. Orrego, J. A. Teixeira, S. I. Mussatto, ‘Encapsulation of antioxidant phenolic compounds extracted from spent coffee grounds by freeze-drying and spray-drying using different coating materials’, Food Chem. 2017, 237, 623–631.
- 13I. Yoplac, L. Vargas, P. Robert, A. Hidalgo, ‘Characterization and antimicrobial activity of microencapsulated citral with dextrin by spray drying’, Heliyon 2021, 7, e06737.
- 14A. G. da Silva Carvalho, M. T. da Costa Machado, V. M. da Silva, A. Sartoratto, R. A. F. Rodrigues, M. D. Hubinger, ‘Physical properties and morphology of spray dried microparticles containing anthocyanins of jussara (Euterpe edulis Martius) extract’, Powder Technol. 2016, 294, 421–428.
- 15J. Righi da Rosa, G. L. Nunes, M. H. Motta, J. P. Fortes, G. C. Cezimbra Weis, L. H. Rychecki Hecktheuer, E. I. Muller, C. Ragagnin de Menezes, C. Severo da Rosa, ‘Microencapsulation of anthocyanin compounds extracted from blueberry (Vaccinium spp.) by spray drying: Characterization, stability and simulated gastrointestinal conditions’, Food Hydrocolloids 2019, 89, 742–748.
- 16R. V. de B Fernandes, E. K. Silva, S. V. Borges, C. R. de Oliveira, M. I. Yoshida, Y. F. da Silva, E. L. do Carmo, V. M. Azevedo, D. A. Botrel, ‘Proposing novel encapsulating matrices for spray-dried ginger essential oil from the whey protein isolate-inulin/maltodextrin blends’, Food Bioprocess Technol. 2017, 10, 115–130.
- 17E. Janiszewska-Turak, N. Dellarosa, U. Tylewicz, L. Laghi, S. Romani, M. Dalla Rosa, D. Witrowa-Rajchert, ‘The influence of carrier material on some physical and structural properties of carrot juice microcapsules’, Food Chem. 2017, 236, 134–141.
- 18D. S. Tupuna, K. Paese, S. S. Guterres, A. Jablonski, S. H. Flôres, A. de O. Rios, ‘Encapsulation efficiency and thermal stability of norbixin microencapsulated by spray-drying using different combinations of wall materials’, Ind. Crops Prod. 2018, 111, 846–855.
- 19X. Hu, B. P. Binks, Z. Cui, ‘High internal phase emulsions stabilized by adsorbed sucrose stearate molecules and dispersed vesicles’, Food Hydrocolloids 2021, 121, 107002.
- 20N. L. Tze, C. P. Han, Y. A. Yusof, C. N. Ling, R. A. Talib, F. S. Taip, M. G. Aziz, ‘Physicochemical and nutritional properties of spray-dried pitaya fruit powder as natural colorant’, Food Sci. Biotechnol. 2012, 21, 675–682.
- 21M. Aghbashlo, H. Mobli, A. Madadlou, S. Rafiee, ‘The correlation of wall material composition with flow characteristics and encapsulation behavior of fish oil emulsion’, Food Res. Int. 2012, 49, 379–388.
- 22R. López-Cruz, J. A. Ragazzo-Sánchez, M. Calderón-Santoyo, ‘Microencapsulation of Meyerozyma guilliermondii by spray drying using sodium alginate and soy protein isolate as wall materials: a biocontrol formulation for anthracnose disease of mango’, Biocontrol Sci. 2020, 30, 1116–1132.
- 23S. Azizi, M. Rezazadeh-Bari, H. Almasi, S. Amiri, ‘Microencapsulation of Lactobacillus rhamnosus using sesame protein isolate: Effect of encapsulation method and transglutaminase’, Food Biosci. 2021, 41, 101012.
- 24S. A. Fioramonti, A. C. Rubiolo, L. G. Santiago, ‘Characterisation of freeze-dried flaxseed oil microcapsules obtained by multilayer emulsions’, Powder Technol. 2017, 319, 238–244.
- 25X. Sun, R. G. Cameron, J. Bai, ‘Effect of spray-drying temperature on physicochemical, antioxidant and antimicrobial properties of pectin/sodium alginate microencapsulated carvacrol’, Food Hydrocolloids 2020, 100, 105420.
- 26S. Barbut, B. A. Harper, ‘Dried Ca-alginate films: Effects of glycerol, relative humidity, soy fibers, and carrageenan’, LWT-Food Sci. Technol. 2019, 103, 260–265.
- 27H. S. Arruda, G. A. Pereira, D. R. de Morais, M. N. Eberlin, G. M. Pastore, ‘Determination of free, esterified, glycosylated and insoluble-bound phenolics composition in the edible part of araticum fruit (Annona crassiflora Mart.) and its by-products by HPLC-ESI-MS/MS’, Food Chem. 2018, 245, 738–749.
- 28V. B. de Souza, M. Thomazini, C. J. De Carvalho Balieiro, C. S. Fávaro-Trindade, ‘Effect of spray drying on the physicochemical properties and color stability of the powdered pigment obtained from vinification byproducts of the Bordo grape (Vitis labrusca)’, Food Bioprod. Process. 2015, 39–50.
- 29G. Caliskan, S. Nur Dirim, ‘The effects of the different drying conditions and the amounts of maltodextrin addition during spray drying of sumac extract’, Food Bioprod. Process. 2013, 91, 539–548.
- 30D. E. Jimenez-Sánchez, M. Calderón-Santoyo, E. Herman-Lara, C. Gaston-Peña, G. Luna-Solano, J. A. Ragazzo-Sánchez, ‘Use of native agave fructans as stabilizers on physicochemical properties of spray-dried pineapple juice’, Drying Technol. 2020, 38, 293–303.
- 31C. G. Greenwald, C. J. King, ‘The effects of design and operating conditions on particle morphology for spray-dried foods’, J. Food Process Eng. 1981, 4, 171–187.
10.1111/j.1745-4530.1981.tb00254.x Google Scholar
- 32K. C. Lee, Y. S. Yoon, F. Z. Li, J. B. Eun, ‘Effects of inlet air temperature and concentration of carrier agents on physicochemical properties, sensory evaluation of spray-dried mandarin (Citrus unshiu) beverage powder’, Appl. Biol. Chem. 2017, 60, 33–40.
- 33A. A. Campos Toledo, J. M. Gomes, E. K. Silva, V. Machado, M. I. Yoshida, S. Vilela, ‘Understanding the influence of encapsulating matrix on the physical and thermal properties of oregano essential oil powder’, Int. J. Hortic. Agric. 2017, 2, 1–8.
- 34M. Cheng, J. Wang, R. Zhang, R. Kong, W. Lu, X. Wang, ‘Characterization and application of the microencapsulated carvacrol/sodium alginate films as food packaging materials’, Int. J. Biol. Macromol. 2019, 141, 259–267.
- 35X. Cai, X. Du, D. Cui, X. Wang, Z. Yang, G. Zhu, ‘Improvement of stability of blueberry anthocyanins by carboxymethyl starch/xanthan gum combinations microencapsulation’, Food Hydrocolloids 2019, 91, 238–245.
- 36X. Pan, P. Sengupta, D. C. Webster, ‘Novel biobased epoxy compounds: Epoxidized sucrose esters of fatty acids’, Green Chem. 2011, 13, 965–975.
- 37D. M. Miss-Zacarías, M. Iñiguez-Moreno, M. Calderón-Santoyo, J. A. Ragazzo-Sánchez, ‘Optimization of ultrasound-assisted microemulsions of citral using biopolymers: characterization and antifungal activity’, J. Dispersion Sci. Technol. 2020, 0, 1–10.
- 38M. Iñiguez-Moreno, J. A. Ragazzo-Sánchez, J. C. Barros-Castillo, J. R. Solís-Pacheco, M. Calderón-Santoyo, ‘Characterization of sodium alginate coatings with Meyerozyma caribbica and impact on quality properties of avocado fruit’, LWT-Food Sci. Technol. 2021, 152, 112346.
- 39V. S. Farias-Cervantes, A. Chávez-Rodríguez, P. A. García-Salcedo, P. M. García-López, J. Casas-Solís, I. Andrade-González, ‘Antimicrobial effect and In Vitro release of anthocyanins from berries and Roselle obtained via microencapsulation by spray drying’, J. Food Process. Preserv. 2018, 42, 1–8.
- 40N. Zhang, Q. Guo, Y. Ma. Stability of anthocyanin in wild blueberry fruit and its degradation kinetics, in Adv. Intell. Soft Comput. Berlin, 2012, p. 539–546.
- 41R. M. A. Daoub, A. H. Elmubarak, M. Misran, E. A. Hassan, M. E. Osman, ‘Characterization and functional properties of some natural Acacia gums’, J. Saudi Soc. Agric. Sci. 2018, 17, 241–249.
- 42S. Jaya, H. Das, ‘Glass transition and sticky point temperatures and stability/mobility diagram of fruit powders’, Food Bioprocess Technol. 2009, 2, 89–95.
- 43D. M. Ferro, C. M. O. Müller, S. R. S. Ferreira, ‘Photostability and characterization of spray-dried maltodextrin powders loaded with Sida rhombifolia extract’, Biocatal. Agric. Biotechnol. 2020, 101716.
- 44J. Ramos-Hernández, J. Ragazzo-Sánchez, M. Calderón-Santoyo, R. I. Ortiz-Basurto, C. Prieto, J. M. Lagaron, ‘Use of electrosprayed agave fructans as nanoencapsulating hydrocolloids for bioactives’, Nanomaterials 2018, 8, 868.
- 45A. López-Rubio, J. M. Lagaron, ‘Whey protein capsules obtained through electrospraying for the encapsulation of bioactives’, Innovative Food Sci. Emerging Technol. 2012, 13, 200–206.
- 46P. S. Negi, G. K. Jayaprakasha, B. S. Jena, ‘Antioxidant and antimutagenic activities of pomegranate peel extracts’, Food Chem. 2003, 80, 393–397.
- 47J. A. Ramos-Hernández, M. Calderón-Santoyo, A. Burgos-Hernández, J. S. García-Romo, A. Navarro-Ocaña, M. G. Burboa-Zazueta, E. Sandoval-Petris, J. A. Ragazzo-Sánchez, ‘Antimutagenic, antiproliferative and antioxidant properties of sea grape leaf extract fractions (Coccoloba uvifera L.)’, Anti-Cancer Agents Med. Chem. 2021, 21, 2250–2257.
- 48G. Ruiz-Montañez, A. Burgos-Hernández, M. Calderón-Santoyo, C. M. López-Saiz, C. A. Velázquez-Contreras, A. Navarro-Ocaña, J. A. Ragazzo-Sánchez, ‘Screening antimutagenic and antiproliferative properties of extracts isolated from Jackfruit pulp (Artocarpus heterophyllus Lam)’, Food Chem. 2015, 175, 409–416.
- 49C. N. Cruz-Salas, C. Prieto, M. Calderón-Santoyo, J. M. Lagarón, J. A. Ramos-Hernández, J. A. Ragazzo-Sánchez, ‘Antimutagenic and antiproliferative activity of the Coccoloba uvifera L. extract loaded in nanofibers of gelatin/agave fructans elaborated by electrospinning’, Anti-Cancer Agents Med. Chem. 2022, 22, 2788–2798.
- 50Hassler, M, ‘Synonymic checklists of the vascular plants of the world′. Ed. O. Bánki, Y. Roskov, M. Döring, G. Ower, L. Vandepitte, D. Hobern, D. Remsen, P. Schalk, R. E. DeWalt, M. Keping, J. Miller, T. Orrell, R. Aalbu, R. Adlard, E. M. Adriaenssens, C. Aedo, E. Aescht, N. Akkari, S. Alexander, et al., Catalogue of Life Checklist (Version 2021–08-06).
- 51D. M. Maron, B. N. Ames, ‘Revised methods for the Salmonella mutagenicity test’, Mutat. Res. Mutagen. Relat. Subj. 1983, 111, 173–215.