Unraveling the antimicrobial activity of nutmeg and turmeric essential oils against Staphylococcus aureus, Listeria monocytogenes, Escherichia coli, and Salmonella spp.
DOI:
https://doi.org/10.5327/fst.00206%20Palavras-chave:
minimum inhibitory concentration, essential oils, microencapsulationResumo
The consumer demand for a reduction in the use of synthetic additives in food has been providing a greater search and incentive for the food industries to use new alternatives for food preservation. Among them, there is the initiative to use essential oils (EOs) due to their antimicrobial properties, coming from specific compounds in their compositions. However, in view of limitations related to the use of EOs, as well as their susceptibility to oxidation and degradation, the possibility arises of employing protection methods such as microencapsulation to minimize the impairment of the benefits associated with the application of EOs. This study aimed to examine the antimicrobial effect of turmeric and nutmeg EOs against microbial strains of Staphylococcus aureus, Listeria monocytogenes, Escherichia coli, and Salmonella spp., as well as the microparticles of the EOs involved. Analyses of the minimum inhibitory concentration (MIC), the minimum bactericidal concentration (MBC), and the developed microparticles, as well as the verification of the synergistic inhibitory action between these oils, were carried out. For free oils, antimicrobial action was evidenced against the vast majority of microorganisms tested, with free nutmeg EO having a better antimicrobial effect than free turmeric oil. In contrast, for encapsulated oils, only antimicrobial action was noted against strains of Listeria. Furthermore, the synergism of free oils did not potentiate the antimicrobial action. Regarding the alternative of microencapsulation of EOs, it was obtained that the results in which chitosan was used as wall material were more promising than when gelatin was used as wall material.
Downloads
Referências
Adams, R. P. (2007). Identification of essential oil components by gas chromatography/mass spectrometry (4th Ed.). Allured Publishing Corporation.
Agibert, S. A. C. (2018). Adição de óleo de amendoim alto oleico encapsulado em chocolate amargo. Universidade de São Paulo.
Ahmed, S. A., Jabbar, I. I., & Abdul, H. E. (2012). Study the Antibacterial Activity of Zingiber officinale roots against Some of Pathogenic Bacteria. Al-Mustansiriyah Journal of Science, 23(3), 63-70.
Akbar, S. (2020). Handbook of 200 Medicinal Plants: A Comprehensive Review of Their Traditional Medical Uses and Scientific Justifications. Springer.
Ali, M. S., Haq, M., Roy, V. C., Ho, T. C., Park, J. S., Han, J. M., & Chun, B.-S. (2023). Development of fish gelatin/carrageenan/zein bio-nanocomposite active-films incorporated with turmeric essential oil and their application in chicken meat preservation. Colloids Surfaces B Biointerfaces, 226, 113320. https://doi.org/10.1016/j.colsurfb.2023.113320
Ansory, H. M., Fitriani, I. N., Nilawatii, A. (2020). Chemical Separation and Antibacterial Activity of Nutmeg seed Essential Oil against Shigella sp. and Escherichia coli ATCC 25922. IOP Conference Series: Materials Science and Engineering, 846(1), 012005. https://doi.org/10.1088/1757-899X/846/1/012005
Antunes, S. A., Robazza, S., Schittler, L., & Gomes, A. (2012). Essential Oil Against Pathogenic Bacteria. Ciência e Tecnologia de Alimentos, 32(3), 525-530. https://doi.org/10.1590/S0101-20612012005000082
Arshad, H., Ali, T. M., Abbas, T., & Hasnain, A. (2018). Effect of Microencapsulation on Antimicrobial and Antioxidant Activity of Nutmeg Oleoresin Using Mixtures of Gum Arabic, OSA, and Native Sorghum Starch. Starch, 70(7-8), 1700320. https://doi.org/10.1002/star.201700320
Ashokkumar, K., Vellaikumar, S., Muthusamy, M., Dhanya, M. K., & Aiswarya, S. (2022). Compositional variation in the leaf, mace, kernel, and seed essential oil of nutmeg (Myristica fragrans Houtt.) from the Western Ghats, India. Natural Product Research, 36(1), 432-435. https://doi.org/10.1080/14786419.2020.1771713
Bauer, K. (1985). Common fragrance and flavor materials: preparation, properties and uses. VCH Verlagsgesellschaft.
da Rosa, M. C., Iacuzio, R., Barbosa, G. R., Pereira, R. C. L., Cruzado-Bravo, M., Rall, V. L. M., Vallim, D. C., & Silva, N. C. C. (2022). Detection of Listeria innocua in the dairy processing chain: resistance to antibiotics and essential oils. Food Science and Technology, 42, e81421. https://doi.org/10.1590/fst.81421
da Silva Cândido, T. J., da Silva, A. C., de Matos, L. G., da Silva do Nascimento, M., Camargo, C. H., Zanella, R. C., Rall, V. L. M., & Silva, N. C. C. (2020). Enterotoxigenic potential and molecular typing of Staphylococcus sp. isolated from organic and conventional fresh Minas cheese in the state of São Paulo, Brazil. International Dairy Journal, 102, 104605. https://doi.org/10.1016/j.idairyj.2019.104605
de Almeida, J. M., Crippa, B. L., de Souza, V. V. M. A., Alonso, V. P. P., da Motta, E. S. J., Picone, C. S. F., Prata, A. S., & Silva, N. C. C. (2023). Antimicrobial action of Oregano, Thyme, Clove, Cinnamon, and Black pepper essential oils free and encapsulated against foodborne pathogens. Food Control, 144, 109356. https://doi.org/10.1016/j.foodcont.2022.109356
de Araújo, R. G. M., Assis, D., Lemes, S. R., de Melo-Reis, P. R., de Araújo, L. A., de Paiva, E. S., & Silva, C. B. (2015). Estudo de caso: Avaliação da atividade antimicrobiana do óleo essencial do açafrão (Curcuma longa). Revista EVS - Revista de Ciências Ambientais e Saúde, 42(4), 425-431. https://doi.org/10.18224/est.v42i4.4361
Dorman, H., & Deans, S. (2000). Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology, 88(2), 308-316. https://doi.org/10.1046/j.1365-2672.2000.00969.x
dos Santos, S. M. (2016). Filmes ativos comestíveis elaborados com óleos essenciais aplicados em maçãs minimamente processadas (Vol. 147). Universidade Federal do Triângulo Mineiro - UFTM Programa.
Ferreira, D. F. (2019). SISVAR: A computer analysis system for fixed effects split-plot type designs. Revista Brasileira de Biometria, 37(4), 529-535. https://doi.org/10.28951/rbb.v37i4.450
Ferreira, F. D., Mossini, S. A. G., Ferreira, F. M. D., Arrotéia, C. C., Costa, C. L. Da, Nakamura, C. V., & Machinski, M. Jr. (2013). The inhibitory effects of Curcuma longa L. essential oil and curcumin on Aspergillus flavus Link growth and morphology. Scientific World Journal, 2013, 343804. https://doi.org/10.1155/2013/343804
Fokou, J. B. H., Dongmo, P. M. J., & Boyom, F. F. (2020). Essential oil’s chemical composition and pharmacological properties. In H. A. El-Shemy (ed.) Essential oils-oils of nature (p. 13). IntechOpen.
Franco, A. L. P., Oliveira, T. B., Ferri, P. H., Bara, M. T. F., & de Paula, J. R. (2007). Avaliação da composição química e atividade antibacteriana dos óleos essenciais de Aloysia gratissima (Gillies & Hook) Tronc. (Alfazema), Ocimum gratissimum L. (Alfavaca-Cravo) E Curcuma longa L. (Açafrão). Revista Eletrônica de Farmácia, 4(2), 208-220. https://doi.org/10.5216/ref.v4i2.3063
Garcia, L. G. S., da Rocha, M. G., Lima, L. R., Cunha, A. P., de Oliveira, J. S., de Andrade, A. R. C., Ricardo, N. M. P. S., Pereira-Neto, W. A., Sidrim, J. J. C., Rocha, M. F. G., Vieira, R. S., & Brilhante, R. S. N. (2021). Essential oils encapsulated in chitosan microparticles against Candida albicans biofilms. International Journal of Biological Macromolecules, 166, 621-632. https://doi.org/10.1016/j.ijbiomac.2020.10.220
Gonçalves, N. D., Grosso, C. R. F., Rabelo, R. S., Hubinger, M. D., & Prata, A. S. (2018). Comparison of microparticles produced with combinations of gelatin, chitosan, and gum Arabic. Carbohydrate Polymers, 196, 427-432. https://doi.org/10.1016/j.carbpol.2018.05.027
Grasso, E. D. C., Aoyama, E. M., & Furlan, M. R. (2017). Ação Anti-inflamatória de Curcuma longa L. (Zingiberaceae). Revista Eletrônica Thesis, 14(28), 117-129.
Hammoud, C. J. (2015). Investigating the inhibitory effects of free and encapsulated curcumin on foodborne pathogens. American University of Beirut.
Hu, Y., Zhang, J., Kong, W., Zhao, G., & Yang, M. (2017). Mechanisms of antifungal and anti-aflatoxigenic properties of essential oil derived from turmeric (Curcuma longa) on Aspergillus flavus. Food Chemistry, 220, 1-8. https://doi.org/10.1016/j.foodchem.2016.09.179
Jansen, P. C. M., & Westphal, E. (Eds.). (1999). Plant Resources of South-East Asia (Vol. 1). Backhuys Publishers.
Khorshidian, N., Yousefi, M., Khanniri, E., & Mortazavian, A. M. (2018). Potential application of essential oils as antimicrobial preservatives in cheese. Innovative Food Science & Emerging Technologies, 45, 62-72. https://doi.org/10.1016/j.ifset.2017.09.020
Knezevic, P., Aleksic, V., Simin, N., Svircev, E., Petrovic, A., & Mimica-Dukic, N. (2016). Antimicrobial activity of Eucalyptus camaldulensis essential oils and their interactions with conventional antimicrobial agents against multi-drug resistant Acinetobacter baumannii. Journal of Ethnopharmacology, 178, 125-136. https://doi.org/10.1016/j.jep.2015.12.008
Kutti Gounder, D., & Lingamallu, J. (2016). Comparison of chemical composition and antioxidant potential of volatile oil from fresh, dried, and cured turmeric (Curcuma longa) rhizomes. Industrial Crops Production, 38, 124-131. https://doi.org/10.1016/j.indcrop.2012.01.014
Laranjo, M., Fernández-Léon, A. M., Potes, M. E., Agulheiro-Santos, A. C., & Elias, M. (2017). Use of Essential Oils in Food Preservation. Antimicrobial Research, 15, 71-84.
Lee, H., Choi, K., Cho, K., & Ahn, Y. (2003). Fungicidal activity of ar-turmerone identified in Curcuma longa rhizome against six phytopathogenic fungi. Agricultural Chemistry Biotechnology, 46(1), 23-28.
Martins, W. D. S., de Araújo, J. S. F., Feitosa, B. F., Oliveira, J. R., Kotzebue, L. R. V., Agostini, D. L. D. S., de Oliveira, D. L. V., Mazzetto, S. E., Cavalcanti, M. T., & da Silva, A. L. (2021). Lemongrass (Cymbopogon citratus DC. Stapf) essential oil microparticles: Development, characterization, and antioxidant potential. Food Chemistry, 355, 129644. https://doi.org/10.1016/j.foodchem.2021.129644
Mendonca, A., Jackson-Davis, A., Moutiq, R., & Thomas-Popo, E. (2018). Use of Natural Antimicrobials of Plant Origin to Improve the Microbiological Safety of Foods. In S. C. Ricke, G. G. Atungulu, C. E. Rainwater, & S. H. Park (ed.). Food and Feed Safety Systems and Analysis (p. 249-272). Elsevier.
Mickus, R., Jančiukė, G., Raškevičius, V., Mikalayeva, V., Matulytė, I., Marksa, M., Maciūnas, K., Bernatonienė, J., & Skeberdis, V. A. (2021). The effect of nutmeg essential oil constituents on Novikoff hepatoma cell viability and communication through Cx43 gap junctions. Biomedicine & Pharmacotherapy, 135, 111229. https://doi.org/10.1016/j.biopha.2021.111229
Morasi, R. M., da Silva, A. Z., Nuñez, K. V. M., Dantas, S. T. A., Faganello, C., Juliano, L. C. B., Tiba-Casas, M. R., Pantoja, J. C. F., Amarante, A. F., Júnior, A. F., Rall, V. L. M., & Silva, N. C. C. (2022). Overview of antimicrobial resistance and virulence factors in Salmonella spp. isolated in the last two decades from chicken in Brazil. Food Research International, 162(part A), 111955. https://doi.org/10.1016/j.foodres.2022.111955
Narasimhan, B., & Dhake, A. S. (2006). Antibacterial principles from Myristica fragrans seeds. Journal of Medicinal Food, 9(3), 395-399. https://doi.org/10.1089/jmf.2006.9.395
Negi, P. S., Chauhan, A. S., Sadia, G. A., Rohinishree, Y. S., & Ramteke, R. S. (2005). Antioxidant and antibacterial activities of various seabuckthorn (Hippophae rhamnoides L.) seed extracts. Food Chemistry, 92(1), 119-124. https://doi.org/10.1016/j.foodchem.2004.07.009
No, H. K., Park, N. Y., Lee, S. H., & Meyers, S. P. (2002). Antibacterial activity of chitosans and chitosan oligomers with different molecular weights. International Journal of Food Microbiology, 74(1-2), 65-72. https://doi.org/10.1016/S0168-1605(01)00717-6
Omoruyi, I. M., & Emefo, O. T. (2012). In vitro evaluation of the antibiogramic activities of the seeds of Myristica fragrans on foodborne pathogens. Malaysian Journal of Microbiology, 8(4), 253-258.
Ouedrhiri, W., Mounyr, B., Harki, E. H., Moja, S., & Greche, H. (2017). Synergistic antimicrobial activity of two binary combinations of marjoram, lavender, and wild thyme essential oils. International Journal of Food Properties, 20(12), 3149-3158. https://doi.org/10.1080/10942912.2017.1280504
Özkan, O. E., Olgun, Ç., Güney, B., Gür, M., Güney, K., & Ates, S. (2018). Chemical composition and antimicrobial activity of Myristica fragrans & Elettaria cardamomum essential oil. Kastamonu Üniversitesi Orman Fakültesi Derg, 18(2), 225-229. https://doi.org/10.17475/kastorman.356765
Paulo, B. B., Schmiele, M., Maximo, G. J., & Prata, A. S. (2019). Carnauba Wax Particles: Investigation of Dripping and Cold-Extrusion Processes. Journal of American Oil Chemists’ Society, 96(7), 847-859. https://doi.org/10.1002/aocs.12224
Prata, A. S., & Grosso, C. R. F. (2015). Production of microparticles with gelatin and chitosan. Carbohydrate Polymers, 116, 292-299. https://doi.org/10.1016/j.carbpol.2014.03.056
Probst, I. D. S. (2012). Atividade antibacteriana de óleos essenciais e avaliação de potencial sinergético. Universidade Estadual Paulista.
Singh, S., Rajesh, B. S. S., Sahoo, K., Subudhi, E., & Nayak, S. (2011). Chemical Composition of Turmeric Oil (Curcuma longa L. cv. Roma) and its Antimicrobial Activity against Eye Infecting Pathogens. Journal of Essential Oil Research, 23(6), 11-18. https://doi.org/10.1080/10412905.2011.9712275
Smith-Palmer, A., Stewart, J., & Fyfe, L. (1998). Antimicrobial properties of plant essential oils and essences against five important food-borne pathogens. Letters Applied Microbiology, 26(2), 118-122. https://doi.org/10.1046/j.1472-765x.1998.00303.x
Takikawa, A., Abe, K., Yamamoto, M., Ishimaru, S., Yasui, M., Okubo, Y., & Yokoigawa, K. (2002). Antimicrobial Activity of Nutmeg against Escherichia coli 0 157. Journal of Bioscience and Bioengineering, 94(4), 315-320. https://doi.org/10.1016/S1389-1723(02)80170-0
Taylor, T. M. (2018). Natural Food Antimicrobials: Recent Trends in Their Use, Limitations, and Opportunities for Their Applications in Food Preservation. In X. Fan, H. Ngo, & C. Wu (ed.). Natural and Bio-Based Antimicrobials for Food Applications (p. 25-43). American Chemical Society Symposium Series.
Thileepan, T., Thevanesam, V., & Kathirgamanathar, S. (2017). Antimicrobial Activity of Seeds and Leaves of Myristica fragrans against Multi-resistant Microorganisms. Journal of Agricultural Science and Technology, 7(5), 302-308. https://doi.org/10.17265/2161-6256/2017.05.002
Valdivieso-Ugarte, M., Gomez-Llorente, C., Plaza-Díaz, J., & Gil, Á. (2019). Antimicrobial, antioxidant, and immunomodulatory properties of essential oils: A systematic review. Nutrients, 11(11), 2786. https://doi.org/10.3390/nu11112786
Wang, Y., Lu, Z., Wu, H., & Lv, F. (2009). Study on the antibiotic activity of microcapsule curcumin against foodborne pathogens. International Journal of Food Microbiology, 136(1), 71-74. https://doi.org/10.1016/j.ijfoodmicro.2009.09.001