Variation in the Phenolic Compounds Profile and Antioxidant Activity in Different Parts of Hawthorn (Crataegus pentagyna Willd.) During Harvest Periods
Jovana Pavlovic 1  
,   Snežana Mitić 1  
,   Milan Mitić 1  
,   Gordana Kocić 2  
,   Aleksandra Pavlović 2  
,   Snežana Tošić 1  
More details
Hide details
Department of Chemistry, Faculty of Science and Mathematics, University of Niš, Višegradska 33, 18000 Niš, Serbia
Department of Biochemistry, Faculty of Medicine, University of Niš, Bulevar dr Zorana Đinđića 81, 18 000 Niš, Serbia
Jovana Pavlovic   

Department of Chemistry, Faculty of Science and Mathematics, University of Nis, Serbia
Submission date: 2018-10-18
Final revision date: 2019-07-17
Acceptance date: 2019-08-29
Online publication date: 2019-11-07
Publication date: 2019-11-18
Pol. J. Food Nutr. Sci. 2019;69(4):367–378
Plants of the genus Crataegus, Rosaceae, are widely distributed and have long been used for food and in folk medicine for the treatment of various ailments. This study focused on HPLC-DAD-FLD identification of phenolic compounds of flowers, fruits, and leaves of hawthorn (Crataegus pentagyna Willd.), on monitoring changes in the content of phenolic compounds during different harvesting periods, as well as on the in vitro testing of the antioxidant activity. Study results showed that neochlorogenic and chlorogenic acids (5.2 and 4.85 mg/g dry weight, respectively) were the most abundant phenolic compounds in the flowers. (-)-Epicatechin and procyanidin B2 were the most abundant phenolic compounds in leaves and fruits. The highest content of phenolic compounds was found in leaves harvested in the early maturity stages, with a tendency of declining in the later stages of maturity. On the other hand, in the case of fruits, the most noticeable changes were found in the content of flavan-3-ols. The highest content of (-)-epicatechin (21.1 mg/g fresh weight) in fruit was in August, and those of procyanidins B2 and B5 in September (10.6 and 3.74 mg/g fresh weight, respectively). Statistical analysis showed a strong correlation between the total phenolics content and the antioxidant activity. This study has demonstrated that there is seasonal variation in both the quantity and the type of phenolic compound as well as the antioxidant activity of different parts of hawthorn.
The research was financed by the Ministry of Education and Science, the Republic of Serbia, projects No. TR 31060 and 45022 internal macro project of Faculty of Sciences and Mathematics, Kosovska Mitrovica.
Albarouki, E., Peterson, A. (2007). Molecular and morphological characterization of Crataegus L. species (Rosaceae) in southern Syria. Botanical Journal of the Linnean Society, 153(3), 255-263.
Amel, B., Seddik, K., Shtaywy, A., Saliha, D., Mussa, A.Z., Assia, B., Saliha, D., Abderahmane, B., Smain, A. (2014). Phytochemical analysis, antioxidant activity and hypotensive effect of Algerian azarole (Crataegus azarolus L.) leaves extracts. Research Journal of Pharmaceutical, Biological and Chemical Science, 5(2), 286-305.
Amira el, A., Behija, S.E., Beligh, M., Lamia, L., Manel, I., Mohamed, H., Lotfi, A. (2012). Effects of the ripening stage on phenolic profile, phytochemical composition and antioxidant activity of date palm fruit. Journal of Agricultural and Food Chemistry, 60(44), 10896-10902.
Apak, R., Güçlü, K., Özyürek, M., Karademir, S.E., Erçağ, E. (2006). The cupric ion reducing antioxidant capacity (CUPRAC) and polyphenolic content of some herbal teas. International Journal of Food Sciences and Nutrition, 57(5-6), 292-304.
Awad, M.A., de Jager, A., van der Plas, L.W.H., van der Krol, A.R. (2001). Flavonoid and chlorogenic acid changes in skin of ‘Elstar’ and ‘Jonagold’ apples during development and ripening. Scientia Horticulturae, 90(1-2), 69-83.
Ben Ahmed, Z., Yousfi, M., Viaene, J., Dejaegher, B., Demeyer, K., Mangelings, D., Heyden, Y.V. (2017). Seasonal, gender and regional variations in total phenolic, flavonoid, and condensed tannins contents and in antioxidant properties from Pistacia atlantica ssp. leaves. Pharmaceutical Biology, 55(1), 1185-1194.
Bernatoniene, J., Masteikova, R., Majiene, D., Savickas, A., Kevelaitis, E., Bernatoniene, R., Dvorácková, K., Civinskiene, G., Lekas, R., Vitkevicius, K., Peciura, R. (2008). Free radical scavenging activities of Crataegus monogyna extracts. Medicina - Lithuania, 44(9), 706-712.
Bleske, B.E., Koch, E., Aaronson, K., Boluyt, M.O. (2008). Hawthorn and heart disease. In R.R. Watson, V.R. Preedy (Eds.), Botanical Medicine in Clinical Practice. CAB International, Wallingford, UK, pp. 493-503.
Brand-Williams, W., Cuvelier, M.E., Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. LWT - Food Science and Technology, 28(1), 25-30.
Bravo, L., Mateos, R. (2008). Analysis of flavonoids in functional foods and nutraceuticals. In W. Jeffrey Hurst (Ed.), Methods of Analysis for Functional Foods and Nutraceuticals, CRC Press, Boca Raton, Florida, USA, pp. 147-207.
Burda, S., Oleszek, W., Lee, C.Y. (1990). Phenolic compounds and their changes in apple during maturation and cold storage. Journal of Agricultural and Food Chemistry, 38(4), 945-948.
Cecarini, V., Gee, J., Fioretti, E., Amici, M., Angeletti, M., Eleuteri, A.M., Keller, J.N. (2007). Protein oxidation and cellular homeostasis: Emphasis on metabolism. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1773(2), 93-104.
Cezarotto, V.S., Giacomelli, S.R., Vendruscolo, M.H., Vestena, A.S., Cezarotto, C.S., da Cruz, R.C., Maurer, L.H., Ferreira, L.M., Emanuelli, T., Cruz, L. (2017). Influence of harvest season and cultivar on the variation of phenolic compounds composition and antioxidant properties in Vaccinium ashei leaves. Molecules, 22(10), art. no. 1603.
Ding, C.K., Chachin, K., Ueda, Y., Imahori, Y., Wang, C.Y. (2001). Metabolism of phenolic compounds during loquat fruit development. Journal of Agricultural and Food Chemistry, 49(6), 2883-2888.
Elmastas, M., Demir, A., Genç, N., Dölek, Ü., Günes, M. (2017). Changes in flavonoid and phenolic acid contents in some Rosa species during ripening. Food Chemistry, 235, 154-159.
Francini, A., Sebastiani, L., (2013). Phenolic compounds in apple (Malus × domestica Borkh.): Compounds characterization and stability during postharvest and after processing. Antioxidants, 2(3), 181-193.
Gao, P.Y., Li, L.Z., Peng, Y., Li, F.F., Niu, C., Huang, X.X., Ming, M., Song, S.J. (2010). Monoterpene and lignan glycosides in the leaves of Crataegus pinnatifida. Biochemical Systematics and Ecology, 38(5), 988-992.
Gucia, M., Jarzyńska, G., Rafal, E., Roszak, M., Kojta, A.K., Osiej, I., Falandysz, J. (2012). Multivariate analysis of mineral constituents of edible Parasol mushroom (Macrolepiota procera) and soils beneath fruiting bodies collected from Northern Poland. Environmental Science and Pollution Research, 19(2), 416-431.
He, F.Y., Li, D.W., Wang, D.M., Deng, M. (2016). Extraction and purification of quercitrin, hyperoside, rutin and afzelin from Zanthoxylum bungeanum Maxim. leaves using a aqueous two-phase system. Journal of Food Science, 81(7), C1593-1602.
Heim, K.E., Tagliaferro, A.R., Bobilya, D.J. (2002). Flavonoid antioxidants, chemistry, metabolism and structure-activity relationship. Journal of Nutritional Biochemistry, 13(10), 572-584.
Hlel, T.B., Belhadj, F., Gül, F., Altun, M., Yağlıoğlu, A.Ş., Demirtaş, I., Marzouki, M.N. (2017). Variations in the bioactive compounds composition and biological activities of Loofah (Luffa cylindrica) fruits in relation to maturation stages. Chemistry and Biodiversity, 14(10), art. no. e1700178.
Huang, D., Ou, B., Prior, R.L. (2005). The chemistry behind antioxidant capacity assays. Journal of Agricultural and Food Chemistry, 53(6), 1841-1856.
Imeh, U., Khokhar, S. (2002). Distribution of conjugated and free phenols in fruits, antioxidant activity and cultivar variations. Journal of Agricultural and Food Chemistry, 50(22), 6301-6306.
Jaakola, L., Määttä, K., Pirttilä, A.M., Torronen, R., Karenlampi, S., Hohtola, A. (2002). Expression of genes involved in anthocyanin biosynthesis in relation to anthocyanin, proanthocyanidin, and flavonol levels during bilberry fruit development. Plant Physiology, 130(2), 729-739.
Kaiser, H.F. (1960). The application of electronic computers to factor analysis. Educational and Psychological Measurement, 20(1), 141-151.
Katalinic, V., Mozina, S. S., Skroza, D., Generalic, I., Abramovic, H., Milos, M., Ljubenkov, I., Piskernik, S., Pezo, I., Terpinc, P., Boban, M. (2010). Polyphenolic profile antioxidant properties and antimicrobial activity of grape skin extract of 14 Vitis vinifera varieties grown in Dalmatia (Croatia). Food Chemistry, 119, 715–723.
Kobayashi, S., Ishimaru, M., Ding, C.K., Yakushiji, H., Goto, N. (2001). Comparison of UDP-glucose, flavonoid 3-O-glucosyltransferase (UFGT) gene sequences between white grapes (Vitis vinifera) and their sports with red skin. Plant Science, 160(3), 543-550.
Krüger, E., Dietrich, H., Hey, M., Patz, C.D. (2011). Effects of cultivar, yield, berry weight, temperature and ripening stage on bioactive compounds of black currants. Journal of Applied Botany and Food Quality, 84, 40-46.
Kumar, D., Arya, V., Bhat, Z.A., Khan, N.A., Prasad, D.A. (2012). The genus Crataegus: chemical and pharmacological perspectives. Revista Brasileira de Farmacognosia, 22(5), 1187-1200.
Lee, C.Y., Kagan, V., Jaworski, A.W., Brown, S.K. (1990). Enzymatic browning in relation to phenolic compounds and polyphenoloxidase activity among various peach cultivars. Journal of Agricultural of Food Chemistry, 38(1), 99-101.
Liu, P., Kallio, H., Yang, B. (2011). Phenolic compounds in hawthorn (Crataegus grayana) fruits and leaves and changes during fruit ripening. Journal of Agricultural and Food Chemistry, 59(20), 11141-11149.
Manning, K. (1998). Isolation of a set ripening-related genes from strawberry, their identification and possible relationship to fruit quality traits. Planta, 205(4), 622-631.
Martz, F., Jaakola, L., Julkunen-Tiitto, R., Stark, S. (2010). Phenolic composition and antioxidant capacity of bilberry (Vaccinium myrtillus) leaves in Northern Europe following foliar development and along environmental gradients. Journal of Chemical Ecology, 36(9), 1017-1028.
Mishra, B., Priyadarsini, K.I., Kumar, M.S., Unnikrishnan, M.K., Mohan, H. (2003). Effect of O-glycosilation on the antioxidant activity and free radical reactions of a plant flavonoid, chrysoeriol. Bioorganic & Medicinal Chemistry, 11(13), 2677-2685.
Mitić, M.N., Souquet, J.M., Obradović, M.V., Mitić, S.S. (2012). Phytochemical profiles and antioxidant activity of Serbian table and wine grapes. Food Science and Biotechnology, 21(6), 1619-1626.
Munhoz, V.M., Longhini, R., Souza, J.R.P., Zequi, J.A.C., Leite Mello, E.V.S., Lopes, G.C., Mello, J.C.P. (2014). Extraction of flavonoids from Tagetes patula: process optimization and screening for biological activity. Revista Brasileira de Farmacognosia, 24(5), 576-583.
Nikolov, N., Batyuk, V.S., Ivanov, V. (1973a). Crateside – A new flavonol glycoside from Crataegus monogyna and C. pentagyna. Chemistry of Natural Compounds, 9(2), 150-151.
Nikolov, N.T., Litvinenko, V.I., Kovalev, I.P. (1973b). Glogoside – A new flavonoid from Crataegus pentagyna. Chemistry of Natural Compounds, 9(2), 144-146.
Nikolov, N.T. (1975). New flavone C-biosides from Crataegus monogyna and Cr. Pentagyna. Chemistry of Natural Compounds, 11(3), 434-435.
Nikolov, N., Seligmann, O., Wagner, H., Horowitz, R.M., Gentili, B. (1982). New flavonoid-glycosides from Crataegus monogyna and Crataegus pentagyna. Planta Medica 44(1), 50-53.
Nurmi, K., Ossipov, V., Haukioja, E., Pihlaja, K. (1996). Variation of total phenolic content and individual low molecular weight phenolics in foliage of mountain birch trees (Betula pubescens spp. tortuosa). Journal of Chemical Ecology, 22(11), 2023-2040.
Oyaizu, M. (1986). Studies on products of browning reaction: Antioxidative activity of products of browning reaction prepared from glucosamine. The Japanese Journal of Nutrition and Dietetics, 44(6), 307-315.
Prinz, S., Ringl, A., Huefner, A., Pemp, E., Kopp, B. (2007). 4'''-Acetylvitexin-2''-O-rhamnoside, isoorientin, orientin, and 8-methoxykaempferol-3-O-glucoside as markers for the differentiation of Crataegus monogyna and Crataegus pentagyna from Crataegus laevigata (Rosaceae). Chemistry & Biodiversity, 4(12), 2920-2931.
Rayyan, S., Fossen, T., Solheim, H.N., Andersen, Ø.M. (2005). Isolation and identification of flavonoids, including flavone rotamers, from the herbal drug (hawthorn). Phytochemical Analysis, 16(5), 334-341.
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 26(9-10), 1231-1237.
Rice-Evans, C. A., Miller, N.J., Paganga, G. (1996). Structure–antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biology and Medicine, 20(7), 933-956.
Rimkiene, L., Kubiliene, A., Zevzikovas, A., Kazlauskiene, D., Jakstas, V. (2017). Variation in flavonoid composition and radical-scavenging activity in Ginkgo biloba L. due to the growth location and time of harvest. Journal of Food Quality, 2017, art. no. 6840397.
Romeyer, F.M., Macheix, J.J., Goiffon, J.P., Reminiac, C.C., Sapis, J.C. (1983). The browning capacity of grapes. 3. Changes and importance of hydroxycinnamic acid-tartaric acid esters during development and maturation of the fruit. Journal of Agricultural and Food Chemistry, 31(2), 346-349.
Routray, W., Orsat, V. (2014). Variation of phenolic profile and antioxidant activity of North American highbush blueberry leaves with variation of time of harvest and cultivar. Industrial Crops and Products, 62, 147-155.
Singleton, V.L., Orthofer, R., Lamuela-Raventos, R.M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Oxidants and Antioxidants, PT A Book Series: Methods in Enzymology, 299, 152-178.
Svedström, U., Vuorela, H., Kostiainen, R., Laakso, I., Hiltunen, R. (2006). Fractionation of polyphenols in hawthorn into polymeric procyanidins, phenolic acids and flavonoids prior to high-performance liquid chromatographic analysis. Journal of Chromatography A, 1112(1-2), 103-111.
Tadić, V.M., Dobrić, S., Marković, G.M., Đorđević, S.M., Arsić, I.A., Menković, N.R., Stević, T. (2008). Anti-inflamatory, gastroprotective, free-radical-scavenging, and antimicrobial activities of hawthorn berries ethanol extract. Journal of Agricultural and Food Chemistry, 56(17), 7700-7709.
Tiwari, U., Cummins, E. (2013). Factors influencing levels of phytochemicals in selected fruit and vegetables during pre- and post-harvest food processing operations. Food Research International, 50(2), SI, 497-506.
Vagiri, M., Conner, S., Stewart, D., Anderson, S.C., Verrall, S., Johansson, E., Rumpunen, K. (2015). Phenolic compounds in blackcurrant (Ribes nigrum L.) leaves relative to leaf position and harvest date. Food Chemistry, 172, 135-142.
Wang, S.Y., Lin, H.S. (2000). Antioxidant activity in fruits and leaves of blackberry, raspberry and strawberry varies with cultivar and development stage. Journal of Agricultural and Food Chemistry, 48(2), 140-146.
Yang, B., Liu, P. (2012). Composition and health effects of phenolic compounds in hawthorn (Crataegus spp.) of different origins. Journal of the Science of Food and Agriculture, 92(8), 1578-1590.
Zhao, H.C., Tian, B.F. (1996). China Fruit-Plant Monograph-Hawthorn Flora. Forestry Publishing House, Bejing, China, p. 366.
Sunflower (Helianthus annuus L.) Plants at Various Growth Stages Subjected to Extraction—Comparison of the Antioxidant Activity and Phenolic Profile
Francesco Gai, Magdalena Karamać, Michał Janiak, Ryszard Amarowicz, Pier Peiretti
Effect of the Growth Stage of False Flax (Camelina sativa L.) on the Phenolic Compound Content and Antioxidant Potential of the Aerial Part of the Plant
Magdalena Karamać, Francesco Gai, Pier Peiretti
Polish Journal of Food and Nutrition Sciences