Abstract
This study was designed within the scope of industrial exploitation of antioxidant extracts from Hibiscus sabdariffa. Efficiency in the extraction of antioxidants (total phenolics, flavonoids and anthocyanins) from calyces was assessed through different processes involving solvents (water, 80% acetone and 80% methanol), microwaves and ultrasounds. Results indicated that microwave extraction with 80% acetone gave the highest yield for total phenolics, expressed as gallic acid equivalents (GAE) per g dry weight (DW) (3.73 GAE/100 g DW), while the highest results for total flavonoids and anthocyanins were found in the microwaved aqueous extracts. Antioxidant activity of the extracts reported the highest reducing power for aqueous extracts with microwave extraction, while 80% acetone and methanol samples exhibited the highest antioxidant activity by high-performance thin-layer chromatography (HPTLC) and 2,2-diphenyl-1-picrylhydrazyl (DPPH) reagent. HPTLC performed for screening of phenolic compounds revealed the occurrence of anthocyanins in dimer-like bands. Laboratory tests showed high protection against lipid oxidation of the whey spread emulsion (22.32 h) incorporated with the sonicated aqueous extract. Results of peptide sequencing data by liquid chromatography electrospray ionization tandem mass spectrometry (LC-ESI-MS/MS), after sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE) analysis, revealed protein–polyphenols interactions by the formation of dimers between polyphenols and protein/peptides. These interactions were found without effect on the oxidative stability of the emulsions. These study suggest that H. sabdariffa’s calyces have the potential to be used like food antioxidants.
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References
Paul, H.: “Hibiscus sabdariffa” L. Paris 5 (1995)
McClintock, N.; El Tahir, I.: Hibiscus sabdariffa L. PROTA 2 (2004)
Hassan, B.H.; Hobani, A.I.: Flow properties of Roselle (Hibiscus sabdariffa L.) extract. J. Food Eng. 35(4), 459–470 (1998). doi:10.1016/S0260-8774(98)00044-2
Endrias, A.: Bio-raffinage de plantes aromatiques et médicinales appliqué à l’Hibiscus sabdariffa L. et à l’Artemisia annua (2006)
Cisse, M.; Dornier, M.; Sakho, M.; Ndiaye, A.; Reynes, M.; Sock, O.: Le bissap (Hibiscus sabdariffa L.): composition et principales utilisations. Fruits 64(03), 179–193 (2009)
Tsai, P.J.; Huang, H.P.; Huang, T.C.: Relationship between anthocyanin patterns and antioxidant capacity in mulberry wine during storage. J. Food Qual. 27(6), 497–505 (2004)
Mendoza-Díaz, S.; Mendoza-Díaz, S.; del Carmen Ortiz-Valerio, M.; Castaño-Tostado, E.; de Dios Figueroa-Cárdenas, J.; Reynoso-Camacho, R.; Ramos-Gómez, M.; Campos-Vega, R.; Loarca-Piña, G.: Antioxidant capacity and antimutagenic activity of anthocyanin and carotenoid extracts from nixtamalized pigmented creole maize races (Zea mays L.). Plant Foods Hum. Nutr. 67(4), 442–449 (2012)
Calligaris, S.; Manzocco, L.; Nicoli, M.C.: Modelling the temperature dependence of oxidation rate in water-in-oil emulsions stored at sub-zero temperatures. Food Chem. 101(3), 1019–1024 (2007). doi:10.1016/j.foodchem.2006.02.056
St Angelo, A.J.: Lipid oxidation in food. In: ACS Symposium Series (USA). American Chemical Society (1992)
Sáyago-Ayerdi, S.G.; Arranz, S.; Serrano, J.; Goñi, I.: Dietary fiber content and associated antioxidant compounds in roselle flower (Hibiscus sabdariffa L.) beverage. J. Agric. Food Chem. 55(19), 7886–7890 (2007)
Bidie, A.; N’guessan, B.; Yapo, A.; N’guessan, J.; Djaman, A.: Activités antioxydantes de dix plantes medicinales de la pharmacopée ivoirienne. Sci. Nat. 8(1–2), 1–12 (2013)
Gu, L.; Zheng, S.; Wu, T.; Chou, G.; Wang, Z.: High-performance thin-layer chromatographic–bioautographic method for the simultaneous determination of Magnolol and Honokiol in Magnoliae officinalis Cortex. JPC-J. Plan. Chromatogr.-Mod. TLC 27(1), 5–10 (2014)
Wang, J.; Cao, X.; Qi, Y.; Ferchaud, V.; Chin, K.L.; Tang, F.: High-performance thin-layer chromatographic method for screening antioxidant compounds and discrimination of Hibiscus sabdariffa L. by principal component analysis. J. Plan. Chromatogr. 28(4), 274–279 (2015)
Cieśla, Ł.; Kryszeń, J.; Stochmal, A.; Oleszek, W.; Waksmundzka-Hajnos, M.: Approach to develop a standardized TLC-DPPH test for assessing free radical scavenging properties of selected phenolic compounds. J. Pharm. Biomed. Anal. 70, 126–135 (2012)
Yrjönen, T.; Peiwu, L.; Summanen, J.; Hopia, A.; Vuorela, H.: Free radical-scavening activity of phenolics by reversed-phase TLC. J. Am. Oil Chem. Soc. 80(1), 9–14 (2003). doi:10.1007/s11746-003-0642-z
Azmir, J.; Zaidul, I.S.M.; Rahman, M.M.; Sharif, K.M.; Mohamed, A.; Sahena, F.; Jahurul, M.H.A.; Ghafoor, K.; Norulaini, N.A.N.; Omar, A.K.M.: Techniques for extraction of bioactive compounds from plant materials: a review. J. Food Eng. 117(4), 426–436 (2013). doi:10.1016/j.jfoodeng.2013.01.014
Li, Y.; Fabiano-Tixier, A.S.; Vian, M.A.; Chemat, F.: Solvent-free microwave extraction of bioactive compounds provides a tool for green analytical chemistry. TrAC Trends Anal. Chem. 47, 1–11 (2013). doi:10.1016/j.trac.2013.02.007
Vinatoru, M.: An overview of the ultrasonically assisted extraction of bioactive principles from herbs. Ultrason. Sonochem. 8(3), 303–313 (2001). doi:10.1016/S1350-4177(01)00071-2
Liu, Q.; Cai, W.; Shao, X.: Determination of seven polyphenols in water by high performance liquid chromatography combined with preconcentration. Talanta 77(2), 679–683 (2008). doi:10.1016/j.talanta.2008.07.011
Ignat, I.; Volf, I.; Popa, V.I.: A critical review of methods for characterisation of polyphenolic compounds in fruits and vegetables. Food Chem. 126(4), 1821–1835 (2011). doi:10.1016/j.foodchem.2010.12.026
Smithers, G.W.: Whey and whey proteins-from ‘gutter-to-gold’. Int. Dairy J. 18(7), 695–704 (2008)
Zall, R.R.: Sources and composition of whey and permeate. In: Zadow, J.G. (ed.) Whey Lactose Process., pp. 1–72. Springer, Netherlands (1992)
Schanbacher, F.L.; Talhouk, R.S.; Murray, F.A.: Biology and origin of bioactive peptides in milk. Livest. Prod. Sci. 50(1–2), 105–123 (1997). doi:10.1016/S0301-6226(97)00082-1
Korhonen, H.; Pihlanto, A.: Bioactive peptides: production and functionality. Int. Dairy J. 16(9), 945–960 (2006). doi:10.1016/j.idairyj.2005.10.012
Onwulata, C.; Huth, P.: Whey Processing, Functionality and Health Benefits, vol. 82. Wiley, New Jersey (2009)
N, Keri Marshall: Therapeutic applications of whey protein. Altern. Med. Rev. 9(2), 136–156 (2004)
Madureira, A.R.; Pereira, C.I.; Gomes, A.M.; Pintado, M.E.; Malcata, F.X.: Bovine whey proteins-overview on their main biological properties. Food Res. Int. 40(10), 1197–1211 (2007)
Bryant, C.M.; McClements, D.J.: Molecular basis of protein functionality with special consideration of cold-set gels derived from heat-denatured whey. Trends Food Sci. Technol. 9(4), 143–151 (1998). doi:10.1016/S0924-2244(98)00031-4
Farrag, A.: Emulsifying and foaming properties of whey protein concentrates in the presence of some carbohydrates. Int. J. Dairy Sci. 3(1), 20–28 (2008)
Herceg, Z.; Režek, A.; Lelas, V.; Krešić, G.; Franetović, M.: Effect of carbohydrates on the emulsifying, foaming and freezing properties of whey protein suspensions. J. Food Eng. 79(1), 279–286 (2007)
Dahmoune, F.; Boulekbache, L.; Moussi, K.; Aoun, O.; Spigno, G.; Madani, K.: Valorization of Citrus limon residues for the recovery of antioxidants: evaluation and optimization of microwave and ultrasound application to solvent extraction. Ind. Crops Prod. 50, 77–87 (2013). doi:10.1016/j.indcrop.2013.07.013
Dahmoune, F.; Spigno, G.; Moussi, K.; Remini, H.; Cherbal, A.; Madani, K.: Pistacia lentiscus leaves as a source of phenolic compounds: microwave-assisted extraction optimized and compared with ultrasound-assisted and conventional solvent extraction. Ind. Crops Prod. 61, 31–40 (2014). doi:10.1016/j.indcrop.2014.06.035
Gülçın, İ.; Oktay, M.; Kıreçcı, E.; Küfrevıoglu, Öİ.: Screening of antioxidant and antimicrobial activities of anise (Pimpinella anisum L.) seed extracts. Food Chem. 83(3), 371–382 (2003). doi:10.1016/S0308-8146(03)00098-0
Djeridane, A.; Yousfi, M.; Nadjemi, B.; Boutassouna, D.; Stocker, P.; Vidal, N.: Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds. Food Chem. 97(4), 654–660 (2006)
Lee, J.; Durst, R.W.; Wrolstad, R.E.: Determination of total monomeric anthocyanin pigment content of fruit juices, beverages, natural colorants, and wines by the pH differential method: collaborative study. J. AOAC Int. 88(5), 1269–1278 (2005)
Simonovska, B.; Vovk, I.; Andrenšek, S.; Valentová, K.; Ulrichová, J.: Investigation of phenolic acids in yacon (Smallanthus sonchifolius) leaves and tubers. J. Chromatogr. A 1016(1), 89–98 (2003). doi:10.1016/S0021-9673(03)01183-X
Gagaoua, M.; Boucherba, N.; Bouanane-Darenfed, A.; Ziane, F.; Nait-Rabah, S.; Hafid, K.; Boudechicha, H.-R.: Three-phase partitioning as an efficient method for the purification and recovery of ficin from Mediterranean fig (Ficus carica L.) latex. Sep. Purif. Technol. 132, 461–467 (2014). doi:10.1016/j.seppur.2014.05.050
Mohd-Esa, N.; Hern, F.S.; Ismail, A.; Yee, C.L.: Antioxidant activity in different parts of roselle (Hibiscus sabdariffa L.) extracts and potential exploitation of the seeds. Food Chem. 122(4), 1055–1060 (2010). doi:10.1016/j.foodchem.2010.03.074
Fernández-Arroyo, S.; Rodríguez-Medina, I.C.; Beltrán-Debón, R.; Pasini, F.; Joven, J.; Micol, V.; Segura-Carretero, A.; Fernández-Gutiérrez, A.: Quantification of the polyphenolic fraction and in vitro antioxidant and in vivo anti-hyperlipemic activities of Hibiscus sabdariffa aqueous extract. Food Res. Int. 44(5), 1490–1495 (2011). doi:10.1016/j.foodres.2011.03.040
Monserrat, J.-P.: Synthèse, caractérisation et criblage biologique de nouveaux dérivés ferrocéniques des flavonoïdes : chalcones, aurones, flavones et flavonols. Université Pierre et Marie Curie - Paris VI (2011)
Sindi, H.A.; Marshall, L.J.; Morgan, M.R.A.: Comparative chemical and biochemical analysis of extracts of Hibiscus sabdariffa. Food Chem. 164, 23–29 (2014). doi:10.1016/j.foodchem.2014.04.097
Prenesti, E.; Berto, S.; Daniele, P.G.; Toso, S.: Antioxidant power quantification of decoction and cold infusions of Hibiscus sabdariffa flowers. Food Chem. 100(2), 433–438 (2007)
Acosta-Estrada, B.A.; Gutiérrez-Uribe, J.A.; Serna-Saldívar, S.O.: Bound phenolics in foods, a review. Food Chem. 152, 46–55 (2014)
Meir, S.; Kanner, J.; Akiri, B.; Philosoph-Hadas, S.: Determination and involvement of aqueous reducing compounds in oxidative defense systems of various senescing leaves. J. Agric. Food Chem. 43(7), 1813–1819 (1995). doi:10.1021/jf00055a012
Albreht, A.; Vovk, I.: Applicability of analytical and preparative monolithic columns to the separation and isolation of major whey proteins. J. Chromatogr. A 1227, 210–218 (2012). doi:10.1016/j.chroma.2012.01.011
Rawel, H.; Kroll, J.; Hohl, U.: Model studies on reactions of plant phenols with whey proteins. Food/Nahrung 45(2), 72–81 (2001)
Yuksel, Z.; Avci, E.; Erdem, Y.K.: Characterization of binding interactions between green tea flavanoids and milk proteins. Food Chem. 121(2), 450–456 (2010). doi:10.1016/j.foodchem.2009.12.064
Hasni, I.; Bourassa, P.; Hamdani, S.; Samson, G.; Carpentier, R.; Tajmir-Riahi, H.-A.: Interaction of milk \(\upalpha \)- and \(\upbeta \)-caseins with tea polyphenols. Food Chem. 126(2), 630–639 (2011). doi:10.1016/j.foodchem.2010.11.087
Kanakis, C.D.; Hasni, I.; Bourassa, P.; Tarantilis, P.A.; Polissiou, M.G.; Tajmir-Riahi, H.-A.: Milk \(\upbeta \)-lactoglobulin complexes with tea polyphenols. Food Chem. 127(3), 1046–1055 (2011). doi:10.1016/j.foodchem.2011.01.079
Rios, M.S.; Santos, F.P.; Maia, F.N.; Mazzetto, S.: Evaluation of antioxidants on the thermo-oxidative stability of soybean biodiesel. J. Therm. Anal. Calorim. 112(2), 921–927 (2013). doi:10.1007/s10973-012-2650-6
Naima, R.; Oumam, M.; Hannache, H.; Sesbou, A.; Charrier, B.; Pizzi, A.; Charrier-El Bouhtoury, F.: Comparison of the impact of different extraction methods on polyphenols yields and tannins extracted from Moroccan Acacia mollissima barks. Ind. Crops Prod. 70, 245–252 (2015). doi:10.1016/j.indcrop.2015.03.016
Pawar, N.; Gandhi, K.; Purohit, A.; Arora, S.; Singh, R.R.B.: Effect of added herb extracts on oxidative stability of ghee (butter oil) during accelerated oxidation condition. J. Food Sci. Technol. 51(10), 2727–2733 (2014). doi:10.1007/s13197-012-0781-1
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Chikhoune, A., Gagaoua, M., Nanema, K.D. et al. Antioxidant Activity of Hibiscus sabdariffa Extracts Incorporated in an Emulsion System Containing Whey Proteins: Oxidative Stability and Polyphenol–Whey Proteins Interactions. Arab J Sci Eng 42, 2247–2260 (2017). https://doi.org/10.1007/s13369-017-2428-z
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DOI: https://doi.org/10.1007/s13369-017-2428-z