Phenolic Content, Antibacterial and Antioxidant Activities of Moroccan propolis

Omar        Belmehdi; Badia         Douhri; Abdelhakim        Bouyahya; Yousif         Laghmouchi; Nadia   S.   Senhaji; Jamal           Abrini

Abstract

Background: Propolis contains compounds with antibacterial and antioxidant capacities, such as phenolic compounds and flavonoids. The aim of this study was to investigate the antibacterial and antioxidant effects of six propolis samples from northern Morocco and to determine their content of polyphenols and flavonoids.

Methods: The total polyphenols and flavonoids of Ethanol Extracts (EEP) were evaluated by colorimetric assays. To test the antibacterial activity, the well diffusion and micro-dilution methods were adopted. The kinetic of bacterial growth in the presence of EEP was tested. The antioxidant activity was evaluated using three techniques: reducing power, β-carotene bleaching test, and DPPH scavenging capacity assay.

Results: The EEPs were found to have high total phenolic content (65.09 - 122.00 mg GAE/g) and flavonoids (41.95 - 50.44 mg QE/g). The screening of the antibacterial activity showed that all tested bacteria were sensitive to EEP except Escherichia coli. The inhibitory zones varied from 11.50 ± 0.70 to 32.00 ± 0.70 mm, and MIC and MBC ranged from 0.07 to 5 mg/mL and 0.07 to >5 mg/mL, respectively. The antioxidant activity was proportional to the phenolic content of propolis. The IC50 varied from 48.70 to 156.00 mg/mL and the RAA% ranged from 75.07 to 96.68 %.

Keywords: Propolis, polyphenols, flavonoids, antibacterial activity, bacterial growth, antioxidant activity.

Graphical Abstract

[1] 
Hegazi, A.G.; Abd El Hady, F.K.; Abd Allah, F.A.M. Chemical composition and antimicrobial activity of European propolis. Z. Natforsch. C J. Biosci.,  2000, 55(1-2), 70-75.
[http://dx.doi.org/10.1515/znc-2000-1-214] 
[2] 
Marcucci, M.C. Propolis: Chemical composition, biological properties and therapeutic activity. Apidologie (Celle),  1995, 26, 83-99.
[http://dx.doi.org/10.1051/apido:19950202] 
[3] 
Remirez, D.; González, R.; Rodriguez, S.; Ancheta, O.; Bracho, J.C.; Rosado, A.; Rojas, E.; Ramos, M.E. Protective effects of Propolis extract on allyl alcohol-induced liver injury in mice. Phytomedicine,  1997, 4(4), 309-314.
[http://dx.doi.org/10.1016/S0944-7113(97)80038-4] 
[4] 
Orsatti, C.L.; Missima, F.; Pagliarone, A.C.; Bachiega, T.F.; Búfalo, M.C.; Araújo, J.P., Jr; Sforcin, J.M. Propolis immunomodulatory action in vivo on Toll-like receptors 2 and 4 expression and on pro-inflammatory cytokines production in mice. Phytother. Res.,  2010, 24(8), 1141-1146.
[5] 
Iyyam Pillai, S.; Palsamy, P.; Subramanian, S.; Kandaswamy, M. Wound healing properties of Indian propolis studied on excision wound-induced rats. Pharm. Biol.,  2010, 48(11), 1198-1206.
[http://dx.doi.org/10.3109/13880200903578754] 
[6] 
Silvestre, N.I.; Stranieri, G.M.; Bazerqu, P.M. Anesthesia (Sollman modified test) of propolis compared with lidocaine. J. Dent. Res.,  1985, 64, 640-640.
[7] 
Keshavarz, K.; Mostafaie, A.; Mansouri, K.; Shakiba, Y.; Motlagh, H.R.M. Inhibition of corneal neovascularization with propolis extract. Arch. Med. Res.,  2009, 40, 59-61.
[http://dx.doi.org/10.1016/j.arcmed.2008.10.004] 
[8] 
Ait Mouse, H.; Tilaoui, M.; Jaafari, A.; Ait M’barek, L.; Aboufatima, R.; Chait, A.; Zyad, A. Evaluation of the in vitro and in vivo anticancer properties of Moroccan propolis extracts. Rev. Bras. Farmacogn.,  2012, 22, 558-567.
[http://dx.doi.org/10.1590/S0102-695X2012005000030] 
[9] 
Marcucci, M.C. Propolis: Chemical composition, biological porperties and therapeutic activity. Apidologie (Celle),  1995, 26, 83-99.
[http://dx.doi.org/10.1051/apido:19950202] 
[10] 
Bankova, V.; De Castro, S.; Marcucci, M. Propolis: Recent advances in chemistry and plant origin. Apidologie (Celle),  2000, 31, 3-15.
[http://dx.doi.org/10.1051/apido:2000102] 
[11] 
Marcucci, M.C.; Bankova, V.S. Chemical composition, plant origin and biological activity of Brazilian propolis. Curr. Topics Phytochem.,  1999, 2, 116-123.
[12] 
Sawaya, A.C.H.F.; Palma, A.M.; Caetano, F.M.; Marcucci, M.C.; da Silva Cunha, I.B.; Araújo, C.E.P.; Shimizu, M.T. Comparative study of in vitro methods used to analyse the activity of propolis extracts with different compositions against species of Candida. Lett. Appl. Microbiol.,  2002, 35(3), 203-207.
[http://dx.doi.org/10.1046/j.1472-765X.2002.01169.x] 
[13] 
Chang, C.; Yang, M.; Wen, H.; Chern, J. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Yao Wu Shi Pin Fen Xi,  2002, 10(3), 178-182.
[14] 
Sforcin, J.M.; Fernandes, A., Jr; Lopes, C.A.M.; Bankova, V.; Funari, S.R.C. Seasonal effect on Brazilian propolis antibacterial activity. J. Ethnopharmacol.,  2000, 73(1-2), 243-249.
[http://dx.doi.org/10.1016/S0378-8741(00)00320-2] 
[15] 
Lu, L.C.; Chen, Y.W.; Chou, C.C. Antibacterial activity of propolis against Staphylococcus aureus. Int. J. Food Microbiol.,  2005, 102(2), 213-220.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2004.12.017] 
[16] 
Vats, S.; Kamal, R. Flavonoids and antioxidant activity of different plant parts and callus Culture of Cassia occidentalis L. Curr. Bioact. Compd.,  2014, 10, 201-206.
[http://dx.doi.org/10.2174/1573407210666140917004952] 
[17] 
Keypour, S.; Mirzania, F.; Farimani, M.M. Antioxidant activity, total flavonoid and phenolic contents of three different extracts of Hyrcanian reishi. Curr. Bioact. Compd.,  2017, 13, 1-5.
[18] 
Vats, S.; Kamal, R. Identification of flavonoids from plant parts and callus culture of Gymnema sylvestre R. Br. An antidiabetic plant. Curr. Bioact. Compd.,  2016, 12, 264-268.
[http://dx.doi.org/10.2174/1573407212666160425150831] 
[19] 
Gülçin, I.; Bursal, E.; Sehitoğlu, M.H.; Bilsel, M.; Gören, A.C. Polyphenol contents and antioxidant activity of lyophilized aqueous extract of propolis from Erzurum, Turkey. Food Chem. Toxicol.,  2010, 48(8-9), 2227-2238.
[http://dx.doi.org/10.1016/j.fct.2010.05.053] 
[20] 
Bahadori, M.B.; Valizadeh, H.; Asghari, B.; Dinparast, L.; Bahadori, S.; Farimani, M.M. Biological activities of Salvia santolinifolia boiss. A multifunctional medicinal plant. Curr. Bioact. Compd.,  2016, 12, 297-305.
[http://dx.doi.org/10.2174/1573407212666160426161112] 
[21] 
Elmastas, M.; Cinkilic, S.; Aboul-Enein, H.Y. New antioxidant source: Matricaria chamomilla. Curr. Bioact. Compd.,  2015, 11, 198-201.
[http://dx.doi.org/10.2174/157340721103151103125058] 
[22] 
Ivanova, D.; Gerova, D.; Chervenkov, T.; Yankova, T. Polyphenols and antioxidant capacity of Bulgarian medicinal plants. J. Ethnopharmacol.,  2005, 96(1-2), 145-150.
[http://dx.doi.org/10.1016/j.jep.2004.08.033] 
[23] 
Awan, K.A.; Butt, M.S.; Haq, I.U.; Suleria, H.A.R. Investigating the antioxidant potential of garlic (Allium sativum) extracts through different extraction modes. Curr. Bioact. Compd.,  2017, 13, 1-6.
[24] 
Siripatrawan, U.; Vitchayakitti, W.; Sanguandeekul, R. Antioxidant and antimicrobial propertoies of Thai propolis extracted using ethanol aqueous solution. Int. J. Food Sci. Technol.,  2013, 48, 22-27.
[http://dx.doi.org/10.1111/j.1365-2621.2012.03152.x] 
[25] 
Mello, B.C.B.S.; Hubinger, M.D. Antioxidant activity and polyphenol contents in Brazilian green propolis extracts prepared with the use of ethanol and water as solvent in different pH values. Int. J. Food Sci. Technol.,  2012, 47, 2510-2518.
[http://dx.doi.org/10.1111/j.1365-2621.2012.03129.x] 
[26] 
Kumazawa, S.; Hamasaka, T.; Nakayama, T. Antioxidant activity of propolis of various geographic origins. Food Chem.,  2004, 84, 329-339.
[http://dx.doi.org/10.1016/S0308-8146(03)00216-4] 
[27] 
Ahn, M.R.; Kunimasa, K.; Kumazawa, S.; Nakayama, T.; Kaji, K.; Uto, Y.; Hori, H.; Nagasawa, H.; Ohta, T. Correlation between antiangiogenic activity and antioxidant activity of various components from propolis. Mol. Nutr. Food Res.,  2009, 53(5), 643-651.
[http://dx.doi.org/10.1002/mnfr.200800021] 
[28] 
Wu, W.M.; Lu, L.; Long, Y.; Wang, T.; Liu, L.; Chen, Q.; Wang, R. Free radical scavenging and antioxidative activity of Caffeic Acid Phenethyl Ester (CAPE) and its related compounds in solution and membranes: A structure-activity insight. Food Chem.,  2007, 105, 107-115.
[http://dx.doi.org/10.1016/j.foodchem.2007.03.049] 
[29] 
Gregoris, E.; Stevanato, R. Correlations between polyphenolic composition and antioxidant activity of Venetian propolis. Food Chem. Toxicol.,  2010, 48(1), 76-82.
[http://dx.doi.org/10.1016/j.fct.2009.09.018] 
[30] 
Miguel, M.G.; Doughmi, O.; Aazza, S.; Antunes, D.; Lyoussi, B. Antioxidant, anti-inflammatory and acetylcholinesterase inhibitory activities of propolis from different regions of Morocco. Food Sci. Biotechnol.,  2014, 23, 313-322.
[http://dx.doi.org/10.1007/s10068-014-0044-1] 
[31] 
Popova, M.; Lyoussi, B.; Aazza, S.; Antunes, D.; Bankova, V.; Miguel, G. Antioxidant and α-Glucosidase inhibitory properties and chemical profiles of Moroccan propolis. Nat. Prod. Commun.,  2015, 10(11), 1961-1964.
[http://dx.doi.org/10.1177/1934578X1501001139] 
[32] 
Singleton, V.L.; Rossi, J.A. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic.,  1965, 16, 144-158.
[33] 
Kalemba, D.; Kunicka, A. Antibacterial and antifungal properties of essential oils. Curr. Med. Chem.,  2003, 10(10), 813-829.
[http://dx.doi.org/10.2174/0929867033457719] 
[34] 
Sarker, S.D.; Nahar, L.; Kumarasamy, Y. Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods,  2007, 42(4), 321-324.
[http://dx.doi.org/10.1016/j.ymeth.2007.01.006] 
[35] 
Campos, J.F.; dos Santos, U.P.; Macorini, L.F.B.; de Melo, A.M.M.F.; Balestieri, J.B.P.; Paredes-Gamero, E.J.; Cardoso, C.A.L.; de Picoli Souza, K.; dos Santos, E.L. Antimicrobial, antioxidant and cytotoxic activities of propolis from Melipona orbignyi (Hymenoptera, Apidae). Food Chem. Toxicol.,  2014, 65, 374-380.
[http://dx.doi.org/10.1016/j.fct.2014.01.008] 
[36] 
Oyaizu, M. Studies on products of browning reactions: Antioxidative activities of products of browning reaction prepared from glucosamine. Japan J. Nutr.,  1986, 44, 307-315.
[http://dx.doi.org/10.5264/eiyogakuzashi.44.307] 
[37] 
Miller, H.E. Simplified method for the evaluation of antioxidant. J. Am. Oil Chem. Soc.,  1971, 13, 380-386.
[http://dx.doi.org/10.1007/BF02635693] 
[38] 
Vokhomina, T.V.; Breeva, L.G.; Bodrova, R.N.; Dushkova, E.S. Some physical and chemical antimicrobial characteristics of propolis and extracts. 22nd Int. Beekeep. Congr. Summ,  1969, pp. 211-217.
[39] 
Campos, V.A.C.; Helvécio, M.J. Oliveir,a D.F.; Walace Carvalho, H.W.P.; Machado, A.R.T.; Tirelli, A.A. Antibacterial activity of propolis produced by Frieseomelitta varia. Cienc. Agrotec.,  2011, 35, 1043-1049.
[http://dx.doi.org/10.1590/S1413-70542011000600002] 
[40] 
Bankova, V.; Christov, R.; Kujumgiev, A.; Marcucci, M.C.; Popov, S. Chemical composition and antibacterial activity of Brazilian propolis. Z. Natforsch. C J. Biosci.,  1995, 50(3-4), 167-172.
[http://dx.doi.org/10.1515/znc-1995-3-402] 
[41] 
Takaisi-Kikuni, N.B.; Schilcher, H. Electron microscopic and microcalorimetric investigations of the possible mechanism of the antibacterial action of a defined propolis provenance. Planta Med.,  1994, 60(3), 222-227.
[http://dx.doi.org/10.1055/s-2006-959463] 
[42] 
Mirzoeva, O.K.; Grishanin, R.N.; Calder, P.C. Antimicrobial action of propolis and some of its components: The effects on growth, membrane potential and motility of bacteria. Microbiol. Res.,  1997, 152(3), 239-246.
[http://dx.doi.org/10.1016/S0944-5013(97)80034-1] 
[43] 
Bryan, J.; Redden, P.; Traba, C. The mechanism of action of Russian propolis ethanol extracts against two antibiotic-resistant biofilm-forming bacteria. Lett. Appl. Microbiol.,  2016, 62(2), 192-198.
[http://dx.doi.org/10.1111/lam.12532] 
[44] 
Shimada, K.; Fujikawa, K.; Yahara, K.; Nakamura, T. Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion. J. Agric. Food Chem.,  1992, 40, 945-948.
[http://dx.doi.org/10.1021/jf00018a005] 
[45] 
Schmidt, E.M.; Stock, D.; Chada, F.J.G.; Finger, D.; Sawaya, A.C.H.F.; Eberlin, M.N.; Felsner, M.L.; Quináia, S.P.; Monteiro, M.C.; Torres, Y.R. A comparison between characterization and biological properties of Brazilian fresh and aged propolis. BioMed Res. Int.,  2014, 2014257617
[http://dx.doi.org/10.1155/2014/257617] 
[46] 
Sanchez-Mareno, C. Review: Methods used to evaluate the free radical scavenging activity in foods and biological systems. Food Sci. Technol. Int.,  2002, 8, 121-137.
[http://dx.doi.org/10.1177/1082013202008003770] 
[47] 
Balogh, E.; Hegedùs, A.; Stefanovits-Banyai, E. Application of and correlation among antioxidant and antiradical assays for characterizing antioxidant capacity of berries. Sci. Hortic. (Amsterdam),  2010, 125, 332-336.
[http://dx.doi.org/10.1016/j.scienta.2010.04.015] 
[48] 
Terpinc, P.; Ceh, B.; Ulrih, N.P.; Abramovic, H. Studies of the correlation between antioxidant properties and the total phenolic content of different oil cake extracts. Ind. Crops Prod.,  2012, 39, 210-217.
[http://dx.doi.org/10.1016/j.indcrop.2012.02.023] 
[49] 
Zhou, K.; Yu, L. Effects of extraction solvent on the wheat bran antioxidant activity estimation. Lebensm. Wiss. Technol.,  2004, 37, 717-721.
[http://dx.doi.org/10.1016/j.lwt.2004.02.008] 

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DOI https://dx.doi.org/10.2174/1573407214666180530100947	Print ISSN 1573-4072
Publisher Name Bentham Science Publisher	Online ISSN 1875-6646

Current Bioactive Compounds

Phenolic Content, Antibacterial and Antioxidant Activities of Moroccan propolis

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