Pitanga and grumixama extracts: antioxidant and antimicrobial activities and incorporation into cellulosic films against Staphylococcus aureus
DOI:
https://doi.org/10.33448/rsd-v9i11.9362Keywords:
Antimicrobial activity; Brazilian fruits; Foodborne microorganisms; Phenolic compounds; S. aureus.Abstract
There is great interest in developing alternatives to improve food safety, since food-borne diseases (FBD) are a major public health concern worldwide. Plant extracts have the potential to inhibit microbial growth due to the action of secondary metabolites, such as phenolic compounds. This study evaluated the antioxidant and antimicrobial activities of phenolic compounds extracted from grumixama (Eugenia brasiliensis) and pitanga (Eugenia uniflora) fruits and the antimicrobial potential of extract of grumixama upon incorporation into cellulosic films. Both fruits were rich in total phenolic compounds and their extracts showed antioxidant activity. The crude and phenolic extracts of grumixama showed higher activity than those isolated from pitanga. All extracts inhibited the growth of Staphylococcus aureus. After incorporation into cellulosic films, the crude extract of grumixama remained active, reducing the S. aureus population in 4 log cycles. The cellulosic films incorporated with grumixama extract were stable after seven days of storage under refrigeration at 7º C; but they partially lost antimicrobial activity when exposed to UV radiation. These phenolic compound-containing cellulosic films could be used as a complementary preservation method of foods that are prone to contamination with S. aureus.
References
Abe, L. T., Lajolo, F. M., & Genovese, M. I. (2012). Potential dietary sources of ellagic acid and other antioxidants among fruits consumed in Brazil: Jabuticaba (Myrciaria jaboticaba (Vell.) Berg). Journal of the Science of Food and Agriculture, 92 (8), 1679-1687. doi: 10.1002/jsfa.5531
Angelo, P. M. & Jorge, N. (2007). Phenolic compounds in foods: a brief review. Revista do Instituto Adolfo Lutz (Impresso), 66 (1), 01-09
Argudín, M. Á., Mendoza, M. C. & Rodicio, M. R. (2010). Food poisoning and Staphylococcus aureus enterotoxins. Toxins, 2 (7), 1751-1773. doi: 10.3390/toxins2071751
Bagetti, M., Facco, E. M. P., Piccolo, J., Hirsch, G. E., Rodriguez-Amaya, D., Kobori, C. N., Vizzotto, M. & Emanuelli, T. (2011). Physicochemical characterization and antioxidant capacity of pitanga fruits (Eugenia uniflora L.). Food Science and Technology, 31 (1), 147-154. doi: 10.1590/S0101-20612011000100021
Bawer, A. W., Kirby, W. M. M., Sherris, J. C. & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45, 493-496. doi: 10.1093/ajcp/45.4_ts.493.
Borges, K. C., Bezerra, M. D. F., Rocha, M. P., Silva, E. S. D., Fujita, A., Genovese, M. I. & Correia, R. T. P. (2016). Fresh and spray dried pitanga (Eugenia uniflora) and jambolan (Syzygium cumini) pulps are natural sources of bioactive compounds with functional attributes. Journal of Probiotics and Health, 4 (2), 1-8. doi: 10.4172/2329-8901.1000145
Bouarab-Chibane, L., Forquet, V., Lantéri, P., Clément, Y., Léonard-Akkari, L., Oulahal, N., Degraeve, P., & Bordes, C. (2019). Antibacterial properties of polyphenols: characterization and QSAR (Quantitative structure–activity relationship) models. Frontiers in Microbiology, 10, 829. doi: 10.3389/fmicb.2019.00829
Brand-Williams, W., Cuvelier, M.E. & Berset, C.L.W.T. (1995). Use of a free radical method to evaluate antioxidant activity. LWT-Food Science and Technology, 28 (1), 25-30. doi: 10.1016/S0023-6438(95)80008-5
Chen, Y., Liu, T., Wang, K., Hou, C., Cai, S., Huang, Y., Du, Z., Huang, H., Kong, J. & Chen, Y. (2016). Baicalein inhibits Staphylococcus aureus biofilm formation and the quorum sensing system in vitro. PLoS One, 11 (4), e0153468. doi: 10.1371/journal.pone.0153468
Chuah, P. N., Nyanasegaram, D., Yu, K. X., Razik, R. M., Al-Dhalli, S., Kue, C. S., Shaari, K. & Ng, C. H. (2020). Comparative conventional extraction methods of ethanolic extracts of Clinacanthus nutans leaves on antioxidant activity and toxicity. British Food Journal, 122 (10), 3139-3149. doi: 10.1108/bfj-02-2020-0085
Cunha, L. R., Soares, N. D. F. F., Assis, F. C. C., Pereira, A. F. & Silva, C. B. (2007). Development and evaluation of active packaging incorporated with lactase. Food Science and Technology, 27 (1), 23-26. doi: 10.1590/S0101-20612007000500004
Cushnie, T. T. & Lamb, A. J. (2011). Recent advances in understanding the antibacterial properties of flavonoids. International Journal of Antimicrobial Agents, 38 (2), 99-107. doi: 10.1016/j.ijantimicag.2011.02.014
Dai, J., Wu, S., Huang, J., Wu, Q., Zhang, F., Zhang, J., Wang, J., Ding, Y., Zhang, S., Yang, X., Lei, T., Xue, L. & Wu, H. (2019). Prevalence and characterization of Staphylococcus aureus isolated from pasteurized milk in China. Frontiers in Microbiology, 10, 641. doi: 10.3389/fmicb.2019.00641
Dannenberg, G. S., Funck, G. D., Cruxen, C. E. S., Marques, J. L., Silva, W. P. & Fiorentini, A.M. (2017). Essential oil from pink pepper as an antimicrobial component in cellulose acetate film: Potential for application as active packaging for sliced cheese. LWT - Food Science and Technology, 81, 314-318. doi: 10.1016/j.lwt.2017.04.002
Ferreira, D. F. (2014). Sisvar: a Guide for its Bootstrap procedure in multiple comparisons. Ciência e Agrotecnologia, 38 (2), 109-112. doi: 10.1590/S1413-70542014000200001
Finger, J. A. F. F., Baroni, W. S. G. V., Maffei, D. F., Bastos, D. H. M. & Pinto, U. M. (2019). Overview of foodborne disease outbreaks in Brazil from 2000 to 2018. Foods, 8 (10), 434. doi: 10.3390/foods8100434
Freitas, M. L. F., Dutra, M. B. L. & Bolini, H. M. A. (2016). Sensory profile and acceptability for pitanga (Eugenia uniflora L.) nectar with different sweeteners. Food and Science Technology International, 22 (8), 720-731. doi: 10.1177/1082013215607077
Garzón, G. A., Soto, C. Y., López-R, M., Riedl, K. M., Browmiller, C. R. & Howard, L. (2020). Phenolic profile, in vitro antimicrobial activity and antioxidant capacity of Vaccinium meridionale Swartz pomace. Heliyon, 6 (5), e03845. doi: 10.1016/j.heliyon.2020.e03845
Gonçalves, A. L., Alves Filho, A. & Menezes, H. (2005). Comparative study on antimicrobial activity of some native tree extracts. Arquivos do Instituto Biológico, 72 (3), 353-358. doi: 10.3109/13880209.2011.596205
Han, J. W., Ruiz‐Garcia, L., Qian, J. P. & Yang, X. T. (2018). Food packaging: A comprehensive review and future trends. Comprehensive Reviews in Food Science and Food Safety, 17 (4), 860-877. doi: 10.1111/1541-4337.12343
Huang, D., Ou, B. & Prior, R. L. (2005). The chemistry behind antioxidant capacity assays. Journal of Agricultural and Food Chemistry, 53 (6), 1841-1856. doi: 10.1021/jf030723c
Infante, J., Rosalen, P. L., Lazarini, J. G., Franchin, M. & Alencar, S. M. (2016). Antioxidant and anti-inflammatory activities of unexplored Brazilian native fruits. PloS One, 11 (4), e0152974. doi: 10.1371/journal.pone.0152974
Kim, D. O., Jeong, S. W. & Lee, C.Y. (2003). Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chemistry, 81 (3), 321-326. doi: 10.1016/S0308-8146(02)00423-5
Lima, V. L. A., Mélo, E. A. & Lima, D. E. S. (2005). The effects of light and freezing temperature upon the stability of purple surinam cherry’s anthocyanin. Food Science and Technology, 25 (1), 92-94. doi: 10.1590/S0101-20612005000100015
Machado, V., Pardo, L., Cuello, D., Giudice, G., Luna, P. C., Varela, G., Camou, T. & Schelotto, F. (2020). Presence of genes encoding enterotoxins in Staphylococcus aureus isolates recovered from food, food establishment surfaces and cases of foodborne diseases. Revista do Instituto de Medicina Tropical de São Paulo, 62, e5. doi: 10.1590/s1678-9946202062005
Minatel, I. O., Borges, C. V., Ferreira, M. I., Gomez, H. A. G., Chen, C. Y. O. & Lima, G. P. P. (2017). Phenolic compounds: Functional properties, impact of processing and bioavailability. In: Soto-Hernandez, M., Palma-Tenango, M. & Garcia-Mateos. Phenolic Compounds - Biological Activity. Rijeka, Croatia: InTech.
Muñoz-Bonilla, A., Echeverria, C., Sonseca, Á., Arrieta, M. P. & Fernández-García, M. (2019). Bio-based polymers with antimicrobial properties towards sustainable development. Materials, 12 (4), 641. doi: 10.3390/ma12040641
Oliveira, L. M. & Oliveira, P. A. P. L. V. (2004). Review: main antimicrobial agents used in plastic packaging. Brazilian Journal of Food Technology, 7 (172), 161-165. Retrieved from
Pessini, G. L., Holetz, F. B., Sanches, N. R., Cortez, D. A. G., Dias Filho, B. P. & Nakamura, C. V. (2003). Avaliação da atividade antibacteriana e antifúngica de extratos de plantas utilizados na medicina popular. Revista Brasileira de Farmacognosia, 13, 21-24. doi: 10.1590/S0102-695X2003000300009
Quecán, B. X. V., Rivera, M. L. C., Hassimotto, N. M. A., Almeida, F. A. & Pinto, U. M. (2019). Effect of quercetin rich onion extracts on bacterial quorum sensing. Frontiers in Microbiology, 10, 867. doi: 10.3389/fmicb.2019.00867
Rais, C., Driouch, A., Slimani, C., Bessi, A., Balouiri, M., El Ghadraoui, L., Lazraq, A. & Figuigui, J. A. (2019). Antimicrobial and antioxidant activity of pulp extracts from three populations of Ziziphus lotus L.. Nutrition & Food Science, 49 (6), 1014-1028. doi: 10.1108/NFS-08-2018-0232
Restrepo, E. A., Rojas, J. D., García, O. R., Sánchez, L. T., Pinzón, M. I. & Villa, C. C. (2018). Mechanical, barrier, and color properties of banana starch edible films incorporated with nanoemulsions of lemongrass (Cymbopogon citratus) and rosemary (Rosmarinus officinalis) essential oils. Food Science and Technology International, 24 (8), 705-712. doi: 10.1177/1082013218792133
Rodrigues, A. C., Zola, F. G., Oliveira, B. D. A., Sacramento, N. T. B., Silva, E. R., Bertoldi, M. C., Taylor, J. G. & Pinto, U. M. (2016). Quorum quenching and microbial control through phenolic extract of Eugenia uniflora fruits. Journal of Food Science, 81 (10), 2538-2544. doi: 10.1111/1750-3841.13431
Salawu, S. O., Ogundare, A. O., Ola-Salawu, B. B. & Akindahunsi, A. A. (2011). Antimicrobial activities of phenolic containing extracts of some tropical vegetables. African Journal of Pharmacy and Pharmacology, 5 (4), 486-492. doi: 10.5897/AJPP10.317
Sánchez-Rangel, J. C., Benavides, J., Heredia, J. B., Cisneros-Zevallos, L. & Jacobo-Velázquez, D. A. (2013). The Folin–Ciocalteu assay revisited: improvement of its specificity for total phenolic content determination. Anal Methods, 5 (21), 5990-5999. doi: 10.1039/c3ay41125g
Santos, C. A., Almeida, F. A., Quecán, B. X. V., Pereira, P. A. P., Gandra, K. M. B., Cunha, L. R. & Pinto, U. M. (2020). Bioactive properties of Syzygium cumini (L.) skeels pulp and seed phenolic extracts. Frontiers in Microbiology, 11, 990. doi: 10.3389/fmicb.2020.00990
Silva, N. C. C., Barbosa, L., Seito, L. N. & Fernandes Junior, A. (2012). Antimicrobial activity and phytochemical analysis of crude extracts and essential oils from medicinal plants. Natural Product Research, 26 (16), 1510-1514. doi: 10.1080/14786419.2011.564582
Silva, N. A. D, Rodrigues, E., Mercadante, A. Z. & Rosso, V. V. (2014). Phenolic compounds and carotenoids from four fruits native from the Brazilian Atlantic forest. Journal of Agricultural and Food Chemistry, 62 (22), 5072-5084. doi: 10.1021/jf501211p
Silva, L. N., Da Hora, G. C. A., Soares, T. A., Bojer, M. S., Ingmer, H., Macedo, A. J. & Trentin, D. S. (2017). Myricetin protects Galleria mellonella against Staphylococcus aureus infection and inhibits multiple virulence factors. Scientific Reports, 7 (1), 1-16. doi: 10.1038/s41598-017-02712-1
Silveira, M. F. A, Soares, N. F. F, Geraldine, R. M., Andrade, N. J. & Gonçalves, M. P. J. (2007). Antimicrobial efficiency and sorbic acid migration from active films into pastry dough. Packaging Technology and Science, 20 (4), 287-292. doi: 10.1002/pts.757
Soares, N. F. F. & Hotchkiss, J. H. (1998). Bitterness reduction in grapefruit juice through active packaging. Packaging Technology and Science, 11 (1), 9-18. doi: doi.org/10.1002/(SICI)1099-1522(199802)11:1<9::AID-PTS413>3.0.CO;2-D
Tayyarcan, E. K., Soykut, E. A., Yilmaz, O. M., Boyaci, I. H., Khaaladi, M. & Fattouch, S. (2019). Investigation of different interactions between Staphylococcus aureus phages and pomegranate peel, grape seed, and black cumin extracts. Journal of Food Safety, 39 (5), e12679. doi: 10.1111/jfs.12679
Tsao, R. (2010). Chemistry and biochemistry of dietary polyphenols. Nutrients, 2 (12), 1231-1246. doi: 10.3390/nu2121231
Waterhouse, A.L. (2002). Determination of total phenolics. Current Protocols in Food Analytical Chemistry, 6 (1) pp. 1-8. doi: 10.1002/0471142913.fai0101s06
WHO - World Health Organization. (2020). Food Safety. Retrieved October, 2020, from https://www.who.int/news-room/fact-sheets/detail/food-safety
Wu, S., Huang, J., Wu, Q., Zhang, F., Zhang, J., Lei, T., Chen, M., Ding, Y. & Xue, L. (2018). Prevalence and characterization of Staphylococcus aureus isolated from retail vegetables in China. Frontiers in Microbiology, 9, 1263. doi: 10.3389/fmicb.2018.01263
Zola, F. G., Rodrigues, A. C., Oliveira, B. D. Á., Sacramento, N. T. B., Taylor, J. G., Pinto, U. M. & Bertoldi, M. C. (2019). Mineral and centesimal contents, antioxidant activity and antimicrobial action of phenolic compounds from Eugenia brasiliensis Lam. Pulp. Food Science and Technology, 39 (2), 378-385. doi: 10.1590/fst.18518
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Copyright (c) 2020 Franciele Mendes de Carvalho ; Jessica Tatiana Aparecida Martins; Emília Maria França Lima; Hellen Vidal Santos; Patrícia Aparecida Pimenta Pereira; Uelinton Manoel Pinto; Luciana Rodrigues da Cunha
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