Effect of physicochemical properties and phenolic compounds of bifloral propolis on antioxidant and antimicrobial capacity

Rey David Vargas Sánchez, Evelin Martínez Benavidez, Javier Hernández, Gastón Ramón Torrescano Urrutia, Armida Sánchez Escalante

Abstract


In this study the effect of pollen source (mesquite and catclaw) on the sensory characteristics (appearance, color, aroma, taste, consistency and visible impurities), and physicochemical properties of raw propolis, and the phenolic content and biological activities of propolis extracts (PEs) was determined. The phenolic composition of PEs was determined by the total phenolic (TPC), flavone and flavonol (FFC), and flavanone and dihydroflavonol content (FDC). The individual phenolic components were analyzed by HPLC-DAD. The antioxidant activity was determined by the ferric-reducing power (FRAP) and free-radical scavenging activity (FRS). The antibacterial activity was evaluated against Gram-positive (Staphylococcus aureus and Listeria innocua) and Gram-negative (Echerichia coli and Salmonella thyphimurium) bacteria. The results showed that sensory characteristic and physicochemical properties of mesquite and catclaw propolis complied with international quality regulations. Fifteen phenolic compounds were identified, of which pinocembrin, naringenin, galangin, chrysin and quercetin were found a high concentration (> 3 mg/g). Mesquite propolis had the highest phenolic content (TFC and FDC), as well as antioxidant activity (> 2.5 mg Fe (II) equivalent/g; > 40% of DPPH radical inhibition) and antibacterial activity against Gram-positive bacterias in the order S. aureus > L. innocua (> 50% of inhibition for both bacterias at 500 µg/mL). These results indicating that pollen source affect the sensory characteristics and physicochemical properties of propolis, as well as the biological activity of their extracts.


Keywords


propolis extract; pollen source; polyphenols; antioxidant; antimicrobial; sensory characteristics; physicochemical properties; bifloral propolis; free-radical; Mesquite propolis; biological activity; pollen

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References


Ainsworth, E. A. & Gillespie, K. M. (2007). Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nature Protocols, 2, 875. DOI: doi:10.1038/nprot.2007.102

Almaraz-Abarca, N., da Graça Campos, M., Avila-Reyes, J. A., Naranjo-Jiménez, N., Corral, J. H. & González-Valdéz, L. S. (2007). Antioxidant activity of polyphenolic extract of monofloral honeybee-collected pollen from mesquite (Prosopis juliflora, Leguminosae). Journal of Food Composition and Analysis, 20, 119-124.

DOI: doi.org/10.1016/j.jfca.2006.08.001

A.O.A.C. (2005). Official Methods of Analysis, 18th ed. Association of Official Analytical Chemists, Gaitherburg, USA.

Bankova, V. S., de Castro, S. L. & Marcucci, M. C. (2000). Propolis: recent advances in chemistry and plant origin. Apidologie, 31, 3-15. DOI: doi.org/10.1051/apido:2000102

Barth, O. M. (1998). Pollen analysis of Brazilian propolis. Grana, 37, 97-101.

DOI: doi.org/10.1080/00173139809362650

Barth, O. M. & da Luz, C. F. P. (2009). Palynological analysis of Brazilian red propolis samples. Journal of Apicultural Research, 48, 181-188. DOI: doi.org/10.3896/IBRA.1.48.3.06

Benzie, I. F. & Strain, J. J. (1999). Ferric reducing antioxidant power assay: Direct measurement of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Method Enzymology, 299, 15-27. DOI: doi.org/10.1016/S0076-6879(99)99005-5

Burdock, G. A. (1998). Review of the biological properties and toxicity of bee propolis (Propolis). Food and Chemical Toxicology, 36, 347-363. DOI: doi.org/10.1016/S0278-6915(97)00145-2

Chaillou, L. L., Herrera, H. A. & Maidana, J. F. (2004). Estudio del propóleos de Santiago del Estero, Argentina. Food Science and Technology (Campinas), 24, 11-15. DOI: dx.doi.org/10.1590/S0101-20612004000100003

Chaillou, L. L. & Nazareno, M. A. (2009). Bioactivity of propolis from Santiago del Estero, Argentina, related to their chemical composition. LWT-Food Science and Technology, 42, 1422-1427. DOI: doi.org/10.1016/j.lwt.2009.03.002

Dias, L. G., Pereira, A. P. & Estevinho, L. M. (2012). Comparative study of different Portuguese samples of propolis: pollinic, sensorial, physicochemical, microbiological characterization and antibacterial activity. Food and Chemical Toxicology, 50, 4246-4253. DOI: doi.org/10.1016/j.fct.2012.08.056

Eumkeb, G., Siriwong, S. & Thumanu, K. (2012). Synergistic activity of luteolin and amoxicillin combination against amoxicillin-resistant Escherichia coli and mode of action. Journal of Photochemistry and Photobiology B: Biology, 117, 247-253.

DOI: doi.org/10.1016/j.jphotobiol.2012.10.006

Farré, R., Frasquet, I. & Sánchez A. (2004). El própolis y la salud. Ars Pharmaceutica, 45, 23-43. http://revistaseug.ugr.es/index.php/ars/article/viewFile/5105/4918

Freire, K. R., Lins, A., Dórea, M. C., Santos, F. A., Cámara, C. A. & Silva, T. (2012). Palynological origin, phenolic content, and antioxidant properties of honeybee-collected pollen from Bahia, Brazil. Molecules, 17, 1652-1664.

DOI: doi.org/10.3390/molecules17021652

Funari, C. S. & Ferro, V. O. (2006). Análise de própolis. Ciência Tecnologia Alimentos, 26, 171-178. http://www.scielo.br/pdf/%0D/cta/v26n1/28867.pdf

Galeotti, F., Maccari, F., Fachini, A. & Volpi, N. (2018). Chemical composition and antioxidant activity of propolis prepared in different forms and in different solvents useful for finished products. Foods, 7, 41. DOI: doi:10.3390/foods7030041

González-Búrquez, M. D. J., González-Díaz, F. R., García-Tovar, C. G., Carrillo-Miranda, L., Soto-Zárate, C. I., Canales-Martínez, M. M., Penieres-Carillo, J. G., Crúz-Sánchez, T. A. & Fonseca-Coronado, S. (2018). Comparison between in vitro antiviral effect of Mexican propolis and three commercial flavonoids against canine distemper virus. Evidence-Based Complementary and Alternative Medicine, 2018. DOI: doi.org/10.1155/2018/7092416

Guzelmeric, E., Ristivojević, P., Trifković, J., Dastan, T., Yilmaz, O., Cengiz, O. & Yesilada, E. (2018). Authentication of Turkish propolis through HPTLC fingerprints combined with multivariate analysis and palynological data and their comparative antioxidant activity. LWT-Food Science and Technology, 87, 23-32. DOI: doi.org/10.1016/j.lwt.2017.08.060

Hernández, J., Goycoolea, F. M., Quintero, J., Acosta, A., Castañeda, M., Domínguez, Z., Robles, R., Vázquez-Moreno, L., Velázquez, E. F., Astiazaran, H., Lugo, E. & Velázquez, C. (2007). Sonoran propolis: chemical composition and antiproliferative activity on cancer cell lines. Planta Medica, 73, 1469-1474. DOI: doi: 10.1055/s-2007-990244

Kalogeropoulos, N., Konteles, S. J., Troullidou, E., Mourtzinos, I. & Karathanos, V. T. (2009). Chemical composition, antioxidant activity and antimicrobial properties of propolis extracts from Greece and Cyprus. Food Chemistry, 116, 452-461.

DOI: doi.org/10.1016/j.foodchem.2009.02.060

Kumazawa, S., Nakamura, J., Murase, M., Miyagawa, M., Ahn, M. R. & Fukumoto, S. (2008). Plant origin of Okinawan propolis: honeybee behavior observation and phytochemical analysis. Naturwissenschaften, 95, 781. DOI: doi: 10.1007/s00114-008-0383-y

LeBlanc, B. W., Davis, O. K., Boue, S., DeLucca, A. & Deeby, T. (2009). Antioxidant activity of Sonoran Desert bee pollen. Food Chemistry, 115, 1299-1305.

DOI: doi.org/10.1016/j.foodchem.2009.01.055

Lozina, L. A., Peichoto, M. E., Acosta, O. C. & Granero, G. E. (2010). Estandarización y caracterización organoléptica y fisicoquímica de 15 propóleos Argentinos. Latin America Journal of Pharmacy, 29, 102-110.

http://www.latamjpharm.org/trabajos/29/1/LAJOP_29_1_1_14_HCS252CF34.pdf

Martins Ribeiro, M. H., da Luz, C. F. P. & de Albuquerque, P. M. C. (2018). Palynology as a tool for distinguishing geopropolis samples from stingless bee species in the Maranhense Amazon, Brazil. Journal of Apicultural Research, 1-21.

DOI: doi.org/10.1080/00218839.2018.1494890

Mašek, T., Perin, N., Racané, L., Cindrić, M., Čipčić Paljetak, H., Perić, M., Matijašić, M., Verbanc, D., Radić, B., Šuran, J. & Starčević, K. (2018). Chemical Composition, antioxidant and antibacterial activity of different extracts of poplar type propolis. Croatica Chemica Acta, 91, 81-88. DOI: doi.org/10.5562/cca3298

Matos, V. R., Alencar, S. M. & Santos, F. A. (2014). Pollen types and levels of total phenolic compounds in propolis produced by Apis mellifera L. (Apidae) in an area of the semiarid region of Bahia, Brazil. Anais da Academia Brasileira de Ciências, 86, 407-418. DOI: dx.doi.org/10.1590/0001-376520142013-0109

Mohamed, S. A. E. S. & Afaf, M. E. S. (2004). Botanical origin of the Sudanese propolis in central areas. University of Kentucky. Journal of Agricultural Science, 12, 9.

Molyneux, P. (2004). The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin Journal of Science and Technology, 26, 211-219. http://www.academia.edu/download/44205041/07-DPPH_1.pdf

Montenegro, G., Peña, R. C., Avila, G. & Timmermann, B. N. (2001). Botanical origin and seasonal production of propolis in hives of Central Chile. Boletim de Botânica da Universidade de São Paulo, 1-6.

https://www.jstor.org/stable/42871506?seq=1#page_scan_tab_contents

Moreira, L., Dias, L. G., Pereira, J. A. & Estevinho, L. (2008). Antioxidant properties, total phenols and pollen analysis of propolis samples from Portugal. Food and Chemical Toxicology, 46, 3482-3485. DOI: doi.org/10.1016/j.fct.2008.08.025

Navarro-Navarro, M., Lugo-Sepúlveda, R. E., García-Moraga, M. C., de la Rosa-López, R., Robles-Zepeda, R. E., Ruiz-Bustos, E. & Velázquez-Contreras, C. (2012). Antibacterial and antioxidant activities of propolis methanolic extracts from Magdalena de Kino and Sonoyta, Sonora. Biotecnia, 14, 9-15. DOI: dx.doi.org/10.18633/bt.v14i3.167

NOA. (2004). Propóleos en bruto. Norma Oficial Argentina IRAM-INTA 15935-1. Buenos Aires, Argentina.

NOM. (2017). Norma Oficial Mexicana NOM-003-SAG/GAN-2017. Propóleos, producción y especificaciones para su procesamiento.

https://normateca.sader.gob.mx/sites/default/files/normateca/Documentos/norma_oficial_mexicana_nom_003_sag_gan_2017_propoleos_produccion_y_especificaciones_para_su_procesamiento.pdf Accessed 11 January 2019.

NSO. (2003). Calidad del propóleos crudo. Norma Salvadoreña 65.19.02:03. NSO 1-12. https://www.oirsa.org/contenido/2017/El_Salvador_INOCUIDAD/8.%20NSO%2065%2019%2002%2003%20-%20CALIDAD_DE_PROPOLEO_CRUDO.pdf Accessed 11 January 2019.

Park, Y. K., Alencar, S. M. & Aguiar, C. L. (2002). Botanical origin and chemical composition of Brazilian propolis. Journal of Agricultural and Food Chemistry, 50, 2502-2506. DOI: doi: 10.1021/jf011432b

Popova, M., Bankova, V., Butovska, D., Petkov, V., Nikolova-Damyanova, B., Sabatini, A. G., Marcazzan, G. L. & Bogdanov, S. (2004). Validated methods for the quantification of biologically active constituents of poplar-type propolis. Phytochemical Analysis, 15, 235-240. DOI: doi.org/10.1002/pca.777

Pratsinis, H., Kletsas, D., Melliou, E. & Chinou, I. (2010). Antiproliferative activity of Greek propolis. Journal of Medicinal Food, 13, 286-290. DOI: doi.org/10.1089/jmf.2009.0071

Ristivojević, P., Dimkić, I., Guzelmeric, E., Trifković, J., Knežević, M., Berić, T., Yesilada, E., Milojković-Opsenica, D. & Stanković, S. (2018). Profiling of Turkish propolis subtypes: Comparative evaluation of their phytochemical compositions, antioxidant and antimicrobial activities. LWT-Food Science and Technology, 95, 367-379. DOI: doi.org/10.1016/j.lwt.2018.04.063

Seidel, V., Peyfoon, E., Watson, D. G. & Fearnley, J. (2008). Comparative study of the antibacterial activity of propolis from different geographical and climate zones. Phytotherapy Research, 22, 1256-1263. DOI: doi.org/10.1002/ptr.2480

Shi, H., Yang, H., Zhang, X. & Yu, L. (2012). Identification and quantification of phytochemical composition and anti-inflammatory and radical scavenging properties of methanolic extracts of Chinese propolis. Journal of Agricultural and Food Chemistry, 60, 12403-12410. DOI: doi: 10.1021/jf3042775

Silici, S., Ünlü, M. & Vardar-Ünlü, G. (2007). Antibacterial activity and phytochemical evidence for the plant origin of Turkish propolis from different regions. World Journal of Microbiology and Biotechnology, 23, 1797-1803. DOI: doi.org/10.1007/s11274-007-9430-7

Vargas-Sánchez, R. D., Torrescano-Urrutia, G. R., Acedo-Félix, E., Carvajal-Millán, E., González-Córdova, A. F., Vallejo-Galland, B., Torres-Llánez, M. J. & Sánchez-Escalante, A. (2014). Antioxidant and antimicrobial activity of commercial propolis extract in beef patties. Journal of Food Science, 79, C1499-C1504. DOI: doi.org/10.1111/1750-3841.12533

Vargas-Sánchez, R. D., Peñalba-Garmendia, M. C., Sánchez-Escalante, J. J., Torrescano-Urrutia, G. R. & Sánchez-Escalante, A. (2016). Pollen profile of propolis produced on the eastern edge of the Sonoran Desert in central Sonora, Mexico. Acta Botánica Mexicana, 114, 69-86. http://www.redalyc.org/articulo.oa?id=57443457004

Viuda‐Martos, M., Ruiz‐Navajas, Y., Fernández‐López, J. & Pérez‐Álvarez, J. A. (2008). Functional properties of honey, propolis, and royal jelly. Journal of Food Science, 73, R117-R124. DOI: doi.org/10.1111/j.1750-3841.2008.00966.x

Wang, X., Hu, H., Luo, Z., Liu, Y. & Zhang, H. (2018). A plant origin of Chinese propolis: Populus canadensis Moench. Journal of Apicultural Research, 57, 228-245. DOI: doi.org/10.1080/00218839.2017.1373512

Wiegand, I., Hilpert, K. & Hancock, R. E. W. (2008). Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nature Protocols, 3, 163-175. DOI: doi:10.1038/nprot.2007.521




DOI: https://doi.org/10.21640/ns.v12i24.2134

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