Health attributes of ten Mediterranean edible flowers: anti-proliferative and enzyme-inhibitory properties

Document Type: Original Article

Authors

Institute of Food Science, CNR-ISA, Via Roma 64, 83100, Avellino, Italy

Abstract

Edible flowers represent an important source of biologically active compounds with positive effects on consumer health. In fact, they contain high quantities of natural antioxidants and have been used since ancient times not only to prepare traditional recipes but also as a remedy against some common illnesses. In the current report, the extracts of ten Mediterranean edible flowers were analyzed to determine their relevant vitamin C, chlorophylls, carotenoids, proanthocyanidins, flavonoids, anthocyanins and total phenolics contents. They were also assayed in vitro for inhibitory effects on digestive enzymes relevant to carbohydrates metabolism and for anti-proliferative activity on CaCo2 colon cancer cell line. Accordingly, the extracts inhibited the a-glucosidase activity in a dose-dependent manner. In addition, half-maximal inhibitory concentration (IC50) ranged from 12.5 ± 1.9 to 132 ± 3.2 mg/mL, while for the anti-proliferative activity IC50 values varied from 24.26 ± 4.5 to 106.3 ± 5.7 mg/mL. In view of the obtained results, the use of these flowers provides important functional ingredients as well as contributing to the realization of delicate and more appealing flavor recipes.

Graphical Abstract

Health attributes of ten Mediterranean edible flowers: anti-proliferative and enzyme-inhibitory properties

Keywords

Main Subjects


Adisakwattana, S. 2017. Cinnamic acid and its derivatives: Mechanisms for prevention and management of diabetes and its complications. Nutrients 9(2), 163.

Bekir, J., Mars, M., Vicendo, P., Fterrich, A., Bouajila, J., 2013. Chemical composition and antioxidant, anti-inflammatory, and antiproliferation activities of pomegranate (Punica granatum) flowers. J. Med. Food 16(6), 544-550.

Davies, S.H.R., Masten, S.J., 1991. Spectrophotometric method for ascorbic acid using dichloro phenolindophenol: elimination of the interference due to iron. Anal. Chim. Acta. 248, 225-227.

Díaz-García, M.C., Castellar, M.R, Obón, J.M., Obón, C., Alcaraz, F., Rivera, D., 2015. Production of an anthocyanin-rich food colourant from Thymus moroderi and its application in foods. J. Sci. Food Agric. 95(6), 1283-1293.

Diplock, A.T., Charleux, J.L., Crozier-Willi, G., Kok, F.J., Rice-Evans, C., Roberfroid, M., Stahl, W., Viña-Ribes, J., 2007. Functional food science and defence against reactive oxidative species. Br. J. Nutr. 80, S77-S112.

Fernandes, L., Casal, S., Pereira, J.A., Saraiva, J.A., Ramalhosa, E. 2017. Edible flowers: A review of the nutritional, antioxidant, antimicrobial properties and effects on human health. J. Food Compost. Anal. 60, 38-50.

Giusti, M.M., Wrolstad, R.E., 2001. Characterization and Measurement of Anthocyanins by UV-Visible Spectroscopy. In Handbook of Food Analytical Chemistry). New Jersey: John Wiley & Sons, pp. 19-31.

Henry-Kirk, R.A., McGhie, T.K., Andre, C.M., Hellens, R.P., Allan, A.C., 2012. Transcriptional analysis of apple fruit proanthocyanidin biosynthesis. J. Exp. Bot. 63(15), 5437-5450.

https://www.r-project.org/.

Kam, A., Li, K.M., Razmovski-Naumovski, V., Nammi, S., Shi, J., Chan, K., Li, G.Q., 2013. A comparative study on the inhibitory effects of different parts and chemical constituents of pomegranate on α-amylase and α-glucosidase. Phytother. Res. 27(11), 1614-1620.

Kee, K.T., Koh, M., Oong, L.X., Ng, K., 2013. Screening culinary herbs for antioxidant and a-glucosidase inhibitory activities. Int. J. Food Sci. Techn. 48(9), 1884-1891.

Langi, P., Kiokias, S., Varzakas, T., Proestos, C., 2018. Carotenoids: from plants to food and feed industries. Methods Mol. Biol. 1852, 57-71.

Levent İnanç, A., 2011. Chlorophyll: Structural properties, health benefits and its occurrence in virgin olive oils. Akademik. Gıda 9(2), 26-32.

Lichtenthaler, H.K., Wellburn, A.R., 1985. Determination of total carotenoids and chlorophylls A and B of leaf in different solvents. Biol. Soc. Trans. 11, 591-592.

Loizzo, M.R., Pugliese, A., Bonesi, M., Tenuta, M.C., Menichini, F., Xiao, J., Tundis, R., 2016. Edible flowers: A rich source of phytochemicals with antioxidant and hypoglycemic properties. J. Agric. Food Chem. 64(12), 2467-2474.

Mazza, G., 2007.Anthocyanins and heart health. Ann. Ist. Super. Sanità. 43, 369-374.

Mellidou, I., Koukounaras, A., Chatzopoulou, F., Kostas, S., Kanellis, A.K., 2017. Plant Vitamin C: One Single Molecule with a Plethora of Roles. Fruit and Vegetable Phytochemicals: Chemistry and Human Health: Second Edition 1, pp. 463-498.

Miguel, M., Barros, L., Pereira, C., Calhelha, R.C., Garcia, P.A., Castro, M., Santos-Buelga, C., Ferreira, I.C., 2016. Chemical characterization and bioactive properties of two aromatic plants: pass L. (flowers) and Mentha cervina L. (leaves). Food Funct. 7(5), 2223-32.

Mishra, V.K., Husen, A., Bachheti, R.K., 2011. Medicinal use of chlorophyll: a critical overview. In: Chlorophyll: Structure, Function and Medicinal Uses, Hua Le and and Elisa Salcedo, Eds., Nova Science Publishers, Inc., Hauppauge, NY 11788 (ISBN 978-162100-015-0), pp.177-196.

Mohammadhosseini, M., 2017. The ethnobotanical, phytochemical and pharmacological properties and medicinal applications of essential oils and extracts of different Ziziphora species. Ind. Crop Prod. 105, 164-192.

Mohammadhosseini, M., Sarker, S.D., Akbarzadeh, A., 2017. Chemical composition of the essential oils and extracts of Achillea species and their biological activities: A review. J. Ethnopharmacol. 199, 257-315.

Mothana, R.A.A., Kriegisch, S., Harms, M., Wende, K., Lindequist, U., 2011. Assessment of selected Yemeni medicinal plants for their in vitro antimicrobial, anticancer, and antioxidant activities. Pharm. Biol. 49(2), 200-210

Ombra, M.N., d'Acierno, A., Nazzaro, F., Riccardi, R., Spigno, P., Zaccardelli, M., Pane, C., Maione, M., Fratianni, F., 2016. Phenolic composition and antioxidant and antiproliferative activities of the extracts of twelve common bean (Phaseolus vulgaris L.) endemic ecotypes of Southern Italy before and after cooking. Oxid. Med. Cell Longev.1398298.

Ombra, M.N., d'Acierno, A., Nazzaro, F., Spigno, P., Riccardi, R., Zaccardelli, M., Pane, C., Coppola, R., Fratianni, F., 2018. Alpha-amylase, α-glucosidase and lipase inhibiting activities of polyphenol-rich extracts from six common bean cultivars of Southern Italy, before and after cooking. Int. J. Food Sci. Nutr. 69(7), 824-834.

Ombra, M.N., Paliogiannis, P., Stucci, L.S., Colombino, M., Casula, M., Sini, M.C., Manca, A., Palomba, G., Stanganelli, I., Mandalà, M., Gandini, S., Lissia, A., Doneddu, V., Cossu, A., Palmieri, G., 2019. Dietary compounds and cutaneous malignant melanoma: Recent advances from a biological perspective. Nutr. Metabol. 16(1), 33.

Pajuelo, D., Quesada, H., Díaz, S., Fernández-Iglesias, A., Arola-Arnal, A., Bladé, C., Salvadó, J., Arola, L., 2012. Chronic dietary supplementation of proanthocyanidins corrects the mitochondrial dysfunction of brown adipose tissue caused by diet-induced obesity in Wistar rats. Br. J. Nutr. 107(2), 170-178.

Pires, T.C.S.P., Dias, M.I., Barros, L., Barreira, J.C.M., Santos-Buelga, C., Ferreira, I.C.F.R., 2018. Incorporation of natural colorants obtained from edible flowers in yogurts. LWT 97, 668-675.

Porter, L.J., Hrstich, L.N., Chan, B.G., 1985. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25, 223-230.

Rauf, A., Imran, M., Abu-Izneid, T., Iahtisham-Ul-Haq, Patel S, Pan X, Naz S, Sanches Silva A, Saeed, F., Rasul, Suleria HA., 2019. Proanthocyanidins: A comprehensive review. Biomed. Pharmacother. 116, 108999.

Saini, R.K., Nile, S.H., Park, S.W., 2015. Carotenoids from fruits and vegetables: Chemistry, analysis, occurrence, bioavailability and biological activities. Food Res. Int. 76(3), 735-750.

Shaji, J., Varkey, D., 2013. Silica-coated solid lipid nanoparticles enhance antioxidant and antiradical effects of meloxicam. J. Pharm. Investig. 43(5), 405-416.

Sharp, H., Hollinshead, J., Bartholomew, B.B., Oben, J., Watson, A., Nash, R.J., 2007. Inhibitory effects of Cissus quadrangularis L. derived components on lipase, amylase and α-glucosidase activity in vitro. Nat. Prod. Commun. 2(8), 817-822.

Singleton, V.L., Rossi, J.A. Jr., 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16, 144-158.

Stintzing, F.C., Carle, R., 2004. functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends Food Sci. Technol. 15, 19-38.

Tanaka, Y., Mochizuki, K., Fukaya, N., Shimada, M., Goda, T. 2009. The α-glucosidase inhibitor miglitol suppresses postprandial hyperglycaemia and interleukin-1β and tumour necrosis factor-α gene expression in rat peripheral leucocytes induced by intermittent sucrose loading. Brit. J. Nutr. 102(2), 221-225.

Thompson, P.L., Davis, T.M.E. 2017. Cardiovascular effects of glucose-lowering therapies for type 2 diabetes: New drugs in perspective. Clin. Ther. 39(5), 1012-1025.

Tomé-Carneiro, J., Visioli, F. 2016. Polyphenol-based nutraceuticals for the prevention and treatment of cardiovascular disease: Review of human evidence. Phytomedicine 23(11), 1145-1174.

Vasic, S.M., Stefanovic, O.D., Licina, B.Z. Radojevic, I.D., Comic, L.R., 2012. Biological activities of extracts from cultivated Granadilla passiflora Alata. EXCLI J. 11, 208-218.

Venditti, A., Frezza, C., Serafini, I., Pulone, S., Scardelletti, G., Sciubba, F., Bianco, A., Serafini, M., 2018. Chemical profiling of the fruits of Styrax officinalis L. from Monti Lucretili (Latium region, Central Italy): Chemotaxonomy and nutraceutical potential. Trends Phytochem. Res. 2(1), 1-12.

Wan, H., Yu, C., Han, Y., Guo, X., Ahmad, S., Tang, A., Wang, J., Cheng, T., Pan, H., Zhang, Q. 2018. Flavonols and carotenoids in yellow petals of rose cultivar (Rosa 'Sun City'): A possible rich source of bioactive compounds. J. Agric. Food Chem. 66(16), 4171-4181.

Xu, Y., Fan, M., Ran, J., Zhang, T., Sun, H., Dong, M., Zhang, Z., Zheng, H., 2016. Variation in phenolic compounds and antioxidant activity in apple seeds of seven cultivars. Saudi J. Biol. Sci. 23(3), 379-388.

Zhishen, J., Mengcheng, T., Jianming, W., 1999. The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem. 64, 555-559.