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Current Bioactive Compounds

Author(s): Danianni M. Zardo, Leydi V.H. Alvarez, Francine G.B. Los, Vivian C. Ito, Ana P. Travalini, Taís Cardoso, José P. Wojeicchoski, Aline Alberti, Acácio A.F. Zielinski, Luís Esmerino and Alessandro Nogueira*

DOI: 10.2174/1573407214666180720123150

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In vitro Assessment of the Antibacterial and Antioxidant Properties of Essential Oils

Page: [592 - 599] Pages: 8

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Abstract

Background: Outbreaks of foodborne diseases cause substantial economic losses. Universities, research institutes and the food industry are increasing their efforts to enhance food safety worldwide. In this context, the study of essential oils as natural antimicrobials and antioxidants for use in foods has become increasingly important.

Methods: The volatile composition and antioxidant and antibacterial activity of Pelargonium graveolens, Cymbopogon citratus, Citrus bergamia, Rosmarinus officinalis and Mentha piperita essential oils were evaluated.

Results: The essential oils showed 80.5 to 95.0% of monoterpenes, but with different profiles. The free radical scavenging activity by the DPPH assay ranged from 3.53 to 68.55% and the total antioxidant potential measured by FRAP ranged from 1.28 to 94.61 mmol TE g-1. The antioxidant activity (FRAP and DPPH assays) of the essential oils followed the order: C. citratus > M. piperita > P. graveolens > C. bergamia > R. officinalis. In general, when the pH tended to neutrality a higher concentration of essential oil was needed to inactivate the microorganisms. The C. citratus oil presented interesting results regarding the inhibition of both strains of S. aureus, showing a lower MIC50 value and Minimum Bactericidal Concentration (MBC) in the concentrations evaluated for E. coli and S. enterica.

Conclusion: The results suggest that C. citratus essential oil has potential as an antibacterial and antioxidant agent.

Keywords: Minimum inhibitory concentration, minimum bactericidal concentration, DPPH, FRAP, Cymbopogon citratus, pH.

Graphical Abstract

[1]
World Health Organization (WHO). WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007-2015.. http://www.who.int/foodsafety/publications/foodborne_disease/fergreport/en/ [Accessed May 05, 2017]
[2]
Food Standards Agency, 2013. Food Standards Agency. Annual report of the chief scientist 2012/13; Food Standards Agency, London, 2013.
[3]
Sistema de informação de agravos de notificação - SINAN. Doenças transmitidas por alimentos: Relatório do Ministério da Saúde (Brasil), portalarquivos.saude.gov.br/.../pdf/2015/.../apresenta---o-dados-gerais-DTA-20152015 [Accessed 07, 2017]
[4]
Diao, W.R.; Hu, Q.P.; Feng, S.S.; Li, W.Q.; Xu, J.G. Chemical composition and antibacterial activity of the essential oil from green huajiao (Zanthoxylum schinifolium) against selected foodborne pathogens. J. Agric. Food Chem., 2013, 61(25), 6044-6049.
[http://dx.doi.org/10.1021/jf4007856] [PMID: 23758080]
[5]
Rashid, S.; Rather, M.A.; Shah, W.A.; Bhat, B.A. Chemical composition, antimicrobial, cytotoxic and antioxidant activities of the essential oil of Artemisia indica Willd. Food Chem., 2013, 138(1), 693-700.
[http://dx.doi.org/10.1016/j.foodchem.2012.10.102] [PMID: 23265542]
[6]
Prado, M.J.G.; Porto, E.; Alencar, S.M.; Gloria, E.M.; Correa, C.B.; Cabral, I.R. Antimicrobial activity of yerba mate (Ilex paraguariensis St. Hil.) against food pathogens. Ver. Argentina de Microbiol., 2013, 45, 93-98.
[http://dx.doi.org/10.1016/S0325-7541(13)70006-3]
[7]
Prado, M.J.G.; Porto, E.; Bani, C.C.; Alencar, S.M.; Gloria, E.M.; Ribeiro, C.I.S.; Aquino, L.M. Antimicrobial potential and chemical composition of agro-industrial wastes. J. Nat. Prod., 2012, 5, 27-39.
[8]
Radha krishnan, K.; Babuskin, S.; Azhagu Saravana Babu, P.; Sasikala, M.; Sabina, K.; Archana, G.; Sivarajan, M.; Sukumar, M. Antimicrobial and antioxidant effects of spice extracts on the shelf life extension of raw chicken meat. Int. J. Food Microbiol., 2014, 171, 32-40.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2013.11.011] [PMID: 24308943]
[9]
Min, K.Y.; Kim, H.J.; Lee, K.A.; Kim, K.T.; Paik, H.D. Antimicrobial activity of acid-hydrolyzed Citrus unshiu peel extract in milk. J. Dairy Sci., 2014, 97(4), 1955-1960.
[http://dx.doi.org/10.3168/jds.2013-7390] [PMID: 24534507]
[10]
Uysal, A.; Gunes, E. Antimicrobial and anti-MRSA effects of three extracts of some Hypericum species against standard microorganisms and methicillin resistant Staphylococcus aureus (MRSA) Strains. Curr. Bioact. Compd., 2015, 11, 146-151.
[http://dx.doi.org/10.2174/1573407211666151002002131]
[11]
Alvarez, F.; Tello, E.; Bauer, K.; Diaz, L.E.; Rodriguez, J.; Jimenez, C. Cytotoxic and antimicrobial diterpenes isolated from Hyptis dilatate. Curr. Bioact. Compd., 2015, 11, 189-197.
[http://dx.doi.org/10.2174/1573407211666150914213356]
[12]
Herman, A.; Tambor, K.; Herman, A. Linalool affects the antimicrobial efficacy of essential oils. Curr. Microbiol., 2016, 72(2), 165-172.
[http://dx.doi.org/10.1007/s00284-015-0933-4] [PMID: 26553262]
[13]
Mattazi, N.; Farah, A.; Fadil, M.; Chraibi, M.; Benbrahim, K.F. Essential oils analysis and antibacterial activity of the leaves of Rosmarinus officinalis, Salvia officinalis and Mentha piperita cultivated in Agadir (Morocco). Int. J. Pharma Sci., 2015, 7, 73-79.
[14]
Mekonnen, A.; Yitayew, B.; Tesema, A.; Taddese, S. In vitro antimicrobial activity of essential oil of Thymus schimperi, Matricaria chamomilla, Eucalyptus globulus, and Rosmarinus officinalis. Int. J. Microbiol., 2016. 20169545693
[http://dx.doi.org/10.1155/2016/9545693] [PMID: 26880928]
[15]
Habbab, A.; Sekkoum, K.; Belboukhari, N.; Cheriti, A.; Aboul-Enein, H.Y. Essential oil chemical composition of Vitex agnus-castus L. from Southern-West Algeria and its antimicrobial activity. Curr. Bioact. Compd., 2016, 12, 51-60.
[http://dx.doi.org/10.2174/1573407212666160330152633]
[16]
Singh, R.; Shushni, M.A.; Belkheir, A. Antibacterial and antioxidant activities of Mentha piperita L. Arab. J. Chem., 2015, 8, 322-328.
[17]
Bertoli, A.; Cirak, C.; Silva, J.A.T. Hypericum species as sources of valuable essential oil. Med. Aromat. Plant Sci. Biotechnol., 2011, 5, 29-47.
[18]
Maida, I.; Lo Nostro, A.; Pesavento, G.; Barnabei, M.; Calonico, C.; Perrin, E.; Chiellini, C.; Fondi, M.; Mengoni, A.; Maggini, V.; Vannacci, A.; Gallo, E.; Bilia, A.R.; Flamini, G.; Gori, L.; Firenzuoli, F.; Fani, R. Exploring the anti-Burkholderia cepacia complex activity of essential oils: A preliminary analysis. Evid. Based Complement. Alternat. Med., 2014. 2014573518
[http://dx.doi.org/10.1155/2014/573518] [PMID: 24701243]
[19]
Joshi, R.K. Chemical composition, in vitro antimicrobial and antioxidant activities of the essential oils of Ocimum gratissimum, O. sanctum and their major constituents. Indian J. Pharm. Sci., 2013, 75(4), 457-462.
[http://dx.doi.org/10.4103/0250-474X.119834] [PMID: 24302801]
[20]
Pérez-Jiménez, J.; Arranz, S.; Tabernero, M.; Díaz-Rubio, M.E.; Serrano, J.; Goñi, I.; Saura-Calixto, F. Updated methodology to determine antioxidant capacity in plant foods, oils and beverages: Extraction, measurement and expression of results. Food Res. Int., 2008, 41, 274-285.
[http://dx.doi.org/10.1016/j.foodres.2007.12.004]
[21]
Brand-Williams, W.; Cuvelier, M.E.; Berset, C.L.W.T. Use of a free radical method to evaluate antioxidant activity. LWT-Food. Sci. Tech. (Paris), 1995, 28, 25-30.
[22]
Benzie, I.F.; Strain, J.J. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Anal. Biochem., 1996, 239(1), 70-76.
[http://dx.doi.org/10.1006/abio.1996.0292] [PMID: 8660627]
[23]
Bassolé, I.H.N.; Lamien-Meda, A.; Bayala, B.; Obame, L.C.; Ilboudo, A.J.; Franz, C.; Novak, J.; Nebié, R.C.; Dicko, M.H. Chemical composition and antimicrobial activity of Cymbopogon citratus and Cymbopogon giganteus essential oils alone and in combination. Phytomedicine, 2011, 18(12), 1070-1074.
[http://dx.doi.org/10.1016/j.phymed.2011.05.009] [PMID: 21665450]
[24]
Antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Approved Standand-Third Edition. CLSI document M31-A3 Wayne, PA., 2008.
[25]
Bakkali, F.; Averbeck, S.; Averbeck, D.; Idaomar, M. Biological effects of essential oils-A review. Food Chem. Toxicol., 2008, 46(2), 446-475.
[http://dx.doi.org/10.1016/j.fct.2007.09.106] [PMID: 17996351]
[26]
Sacchetti, G.; Maietti, S.; Muzzoli, M.; Scaglianti, M.; Manfredini, S.; Radice, M.; Bruni, R. Comparative evaluation of 11 essential oils of different origin as functional antioxidants, antiradicals and antimicrobials in foods. Food Chem., 2005, 91, 621-632.
[http://dx.doi.org/10.1016/j.foodchem.2004.06.031]
[27]
Mimica-Dukić, N.; Božin, B.; Soković, M.; Mihajlović, B.; Matavulj, M. Antimicrobial and antioxidant activities of three Mentha species essential oils. Planta Med., 2003, 69(5), 413-419.
[http://dx.doi.org/10.1055/s-2003-39704] [PMID: 12802721]
[28]
Choi, H.S.; Song, H.S.; Ukeda, H.; Sawamura, M. Radical-scavenging activities of citrus essential oils and their components: detection using 1,1-diphenyl-2-picrylhydrazyl. J. Agric. Food Chem., 2000, 48(9), 4156-4161.
[http://dx.doi.org/10.1021/jf000227d] [PMID: 10995330]
[29]
Wei, A.; Shibamoto, T. Antioxidant/lipoxygenase inhibitory activities and chemical compositions of selected essential oils. J. Agric. Food Chem., 2010, 58(12), 7218-7225.
[http://dx.doi.org/10.1021/jf101077s] [PMID: 20499917]
[30]
Prado Martin, J.G.; Porto, E.; de Alencar, S.M.; da Glória, E.M.; Corrêa, C.B.; Ribeiro Cabral, I.S. Antimicrobial activity of yerba mate (Ilex paraguariensis St. Hil.) against food pathogens. Rev. Argent. Microbiol., 2013, 45(2), 93-98.
[http://dx.doi.org/10.1016/S0325-7541(13)70006-3] [PMID: 23876271]
[31]
Stanetic, D.; Buchbauer, G. Biological activity of some volatile diterpenoids. Curr. Bioact. Compd., 2015, 11, 38-48.
[http://dx.doi.org/10.2174/157340721101150804150419]
[32]
Smith-Palmer, A.; Stewart, J.; Fyfe, L. The potential application of plant essential oils as natural food preservatives in soft cheese. Food Microbiol., 2001, 18, 463-470.
[http://dx.doi.org/10.1006/fmic.2001.0415]
[33]
Naik, M.I.; Fomda, B.A.; Jaykumar, E.; Bhat, J.A. Antibacterial activity of lemongrass (Cymbopogon citratus) oil against some selected pathogenic bacterias. Asian Pac. J. Trop. Med., 2010, 3, 535-538.
[http://dx.doi.org/10.1016/S1995-7645(10)60129-0]
[34]
Burt, S. Essential oils: Their antibacterial properties and potential applications in foods-S review. Int. J. Food Microbiol., 2004, 94(3), 223-253.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2004.03.022] [PMID: 15246235]
[35]
Deans, S.G.; Ritchie, G. Antibacterial properties of plant essential oils. Int. J. Food Microbiol., 1987, 5, 165-180.
[http://dx.doi.org/10.1016/0168-1605(87)90034-1]
[36]
Fisher, K.; Phillips, C.A. The effect of lemon, orange and bergamot essential oils and their components on the survival of Campylobacter jejuni, Escherichia coli O157, Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus in vitro and in food systems. J. Appl. Microbiol., 2006, 101(6), 1232-1240.
[http://dx.doi.org/10.1111/j.1365-2672.2006.03035.x] [PMID: 17105553]
[37]
Tassou, C.C.; Nychas, G.J.E. Antimicrobial activity of the essential oil of mastic gum (Pistacia lentiscus var. chia) on Gram positive and Gram negative bacteria in broth and in model food system. Int. Biodet. Biodeg., 1995, 36, 411-420.
[http://dx.doi.org/10.1016/0964-8305(95)00103-4]
[38]
Sienkiewicz, M.; Poznańska-Kurowska, K.; Kaszuba, A.; Kowalczyk, E. The antibacterial activity of geranium oil against Gram-negative bacteria isolated from difficult-to-heal wounds. Burns, 2014, 40(5), 1046-1051.
[http://dx.doi.org/10.1016/j.burns.2013.11.002] [PMID: 24290961]
[39]
Sandasi, M.; Leonard, C.M.; van Vuuren, S.F.; Viljoen, A.M. Peppermint (Mentha piperita) inhibits microbial biofilms in vitro. S. Afr. J. Bot., 2011, 77, 80-85.
[http://dx.doi.org/10.1016/j.sajb.2010.05.011]
[40]
Saharkhiz, M.J.; Motamedi, M.; Zomorodian, K.; Pakshir, K.; Miri, R.; Hemyari, K. Chemical composition, antifungal and antibiofilm activities of the essential oil of Mentha piperita L. ISRN Pharm., 2012. 2012718645
[http://dx.doi.org/10.5402/2012/718645] [PMID: 23304561]
[41]
Yadegarinia, D.; Gachkar, L.; Rezaei, M.B.; Taghizadeh, M.; Astaneh, S.A.; Rasooli, I. Biochemical activities of Iranian Mentha piperita L. and Myrtus communis L. essential oils. Phytochemistry, 2006, 67(12), 1249-1255.
[http://dx.doi.org/10.1016/j.phytochem.2006.04.025] [PMID: 16777154]
[42]
Elmann, A.; Mordechay, S.; Rindner, M.; Ravid, U. Anti-neuroinflammatory effects of geranium oil in microglial cells. J. Funct. Foods, 2010, 2, 17-22.
[http://dx.doi.org/10.1016/j.jff.2009.12.001]
[43]
Moufida, S.; Marzouk, B. Biochemical characterization of blood orange, sweet orange, lemon, bergamot and bitter orange. Phytochemistry, 2003, 62(8), 1283-1289.
[http://dx.doi.org/10.1016/S0031-9422(02)00631-3] [PMID: 12648552]
[44]
Fisher, K.; Phillips, C. Potential antimicrobial uses of essential oils in food: Is citrus the answer? Trends Food Sci. Technol., 2008, 19, 156-164.
[http://dx.doi.org/10.1016/j.tifs.2007.11.006]
[45]
Benvenuti, F.; Gironi, F.; Lamberti, L. Supercritical deterpenation of lemon essential oil, experimental data and simulation of the semicontinuous extraction process. J. Supercrit. Fluids, 2001, 20, 29-44.
[http://dx.doi.org/10.1016/S0896-8446(01)00058-4]
[46]
Paradella, T.C.; Koga-Ito, C.Y.; Jorge, A.O.C. Enterococcus faecalis: considerações clínicas e microbiológicas. Rev. Odontol. UNESP, 2007, 36, 163-168.
[47]
Tyagi, A.K.; Malik, A. Antimicrobial potential and chemical composition of Mentha piperita oil in liquid and vapour phase against food spoiling microorganisms. Food Control, 2011, 22, 1707-1714.
[http://dx.doi.org/10.1016/j.foodcont.2011.04.002]
[48]
Celiktas, O.Y.; Kocabas, E.H.; Bedir, E.; Sukan, F.V.; Ozek, T.; Baser, K.H.C. Antimicrobial activities of methanol extracts and essential oils of Rosmarinus officinalis, depending on location and seasonal variations. Food Chem., 2007, 100, 553-559.
[http://dx.doi.org/10.1016/j.foodchem.2005.10.011]
[49]
Turgis, M.; Han, J.; Caillet, S.; Lacroix, M. Antimicrobial activity of mustard essential oil against Escherichia coli O157: H7 and Salmonella typhi. Food Control, 2009, 20, 1073-1079.
[http://dx.doi.org/10.1016/j.foodcont.2009.02.001]
[50]
Okoh, O.O.; Sadimenko, A.P.; Afolayan, A.J. Comparative evaluation of the antibacterial activities of the essential oils of Rosmarinus officinalis L. obtained by hydrodistillation and solvent free microwave extraction methods. Food Chem., 2010, 120, 308-312.
[http://dx.doi.org/10.1016/j.foodchem.2009.09.084]
[51]
Dorman, H.J.D.; Deans, S.G. Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J. Appl. Microbiol., 2000, 88(2), 308-316.
[http://dx.doi.org/10.1046/j.1365-2672.2000.00969.x] [PMID: 10736000]