Abstract
Most studies evaluating the use of essential oils (EO) as antibacterial agents focus mainly on minimal inhibitory concentrations (MIC) rather than minimal bactericidal concentrations (MBC). In this work, we compared MICs and MBCs of EO from condiment plants commonly used in Mediterranean Europe, namely Origanum vulgare, Salvia lavandulaefolia, Salvia officinalis, Salvia sclarea and Rosmarinus officinalis, aiming to evaluate their application as disinfecting agents in minimally processed produce. Outbreaks-related pathogens such as Listeria monocytogenes, Pseudomonas aeruginosa and Yarrowia lipolytica were used. Results showed that all EO were able to reduce bacterial growth in all bacterial strains tested, particularly O. vulgare. However, fewer EO exhibited bactericidal activities, and were only effective against one or two bacterial strains, hence eliminating the possibility to use them as broad range disinfectants. Furthermore, the necessary concentrations were too high for food application. Hence, our work suggests the need to evaluate MBC rather than MIC and questions EO usefulness in controlling undesired microorganisms. Overall, and despite the large volume of data published on EO, results obtained were not very encouraging for a realistic application on produce and question the viability of EOs as disinfecting agents in food.
Similar content being viewed by others
References
Azevedo AN, Buarque PR, Cruz EMO, Blank AF, Alves PB, Nunes ML, Santana LCLA (2014) Response surface methodology for optimization of edible chitosan coating formulations incorporating essential oil against several foodborne pathogenic bacteria. Food Control 43:1–9. doi:10.1016/j.foodcont.2014.02.033
Bakkali F (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475. doi:10.1016/j.fct.2007.09.106
Bouhdid S, Abrini J, Amensour M, Zhiri A, Espuny M, Manresa A (2010) Functional and ultrastructural changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Cinnamomum verum essential oil. J Appl Microbiol 109:1139–1149. doi:10.1111/j.1365-2672.2010.04740.x
Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods-a review. Int J Food Microbiol 94:223–253. doi:10.1016/j.ijfoodmicro.2004.03.022
Callejón RM, Rodríguez-Naranjo MI, Ubeda C, Hornedo-Ortega R, Garcia-Parrilla MC, Troncoso AM (2015) Reported foodborne outbreaks due to fresh produce in the United States and European Union: trends and causes. Foodborne Pathog Dis 12:32–38. doi:10.1089/fpd.2014.1821
Cleff MB, Meinerz AR, Xavier M, Schuch LF, Meireles MCA, Rodrigues MRA, Mello JRB (2010) In vitro activity of Origanum vulgare essential oil against Candida species. Braz J Microbiol 41:116–123. doi:10.1590/S1517-838220100001000018
Cosentino S, Tuberoso CIG, Pisano B, Satta M, Mascia V, Arzedi E, Palmas F (1999) In-vitro antimicrobial activity and chemical composition of Sardinian Thymus essential oils. Lett Appl Microbiol 29:130–135
De Martino L, De Feo V, Formisano C, Mignola E, Senatore F (2009) Chemical Composition and Antimicrobial Activity of the Essential Oils from Three Chemotypes of Origanum vulgare L.ssp. hirtum (Link) Ietswaart Growing Wild in Campania (Southern Italy). Molecules 14:2735–2746. doi:10.3390/molecules14082735
Dehkordi SSS, Rohani SMR, Tajik H, Moradi M, Aliakbarlou J (2008) Antimicrobial effects of lysozyme in combination with Zataria multiflora Boiss. essential oil at different pH and NaCl concentrations on E. coli O157:H7 and Staphylococcus aureus. J Anim Vet Adv 7:1458–1463. http://medwelljournals.com/abstract/?doi=javaa.2008.1458.1463. Accessed 5 May 2016
Dobre A, Gagiu V, Petru N (2011) Antimicrobial activity of essential oils against food-borne bacteria evaluated by two preliminary methods. Rom Biotech Lett 16:119–125. https://www.rombio.eu/rbl6vol16Supplement/18%20Dobre%20Alina.pdf. Accessed 7 July 2016
Faleiro ML, Miguel MG, Ladeiro F, Venâncio F, Tavares R, Brito JC, Figueiredo AC, Barroso JG, Pedro LG (2003) Antimicrobial activity of essential oils isolated from Portuguese endemic species of Thymus. Lett Appl Microbiol 36:35–40. doi:10.1046/j.1472-765X.2003.01259.x
Frangos L, Pyrgotou N, Giatrakou V, Ntzimani A, Savvaidis IN (2010) Combined effects of salting, oregano oil and vacuum-packaging on the shelf-life of refrigerated trout fillets. Food Microbiol 27:115–121. doi:10.1016/j.fm.2009.09.002
Gachkar L, Yadegari D, Rezaei MB, Taghizadeh M, Astaneh SA, Rasooli I (2007) Chemical and biological characteristics of Cuminum cyminum and Rosmarinus officinalis essential oils. Food Chem 102:898–904. doi:10.1016/j.foodchem.2006.06.035
Gil MI, Selma MV, López-Gálvez F, Allende A (2009) Fresh-cut product sanitation and wash water disinfection: problems and solutions. Int J Food Microbiol 134:37–45. doi:10.1016/j.ijfoodmicro.2009.05.021
Guerreiro AC, Gago CML, Faleiro ML, Miguel MGC, Antunes MDC (2015) Raspberry fresh fruit quality as affected by pectin and alginate-based edible coatings enriched with essential oils. Sci Hort 194:138–146. doi:10.1016/j.scienta.2015.08.004
Karagözlü N, Ergönül B, Özcan D (2011) Determination of antimicrobial effect of mint and basil essential oils on survival of E. coli O157:H7 and S. typhimurium in fresh-cut lettuce and purslane. Food Control 22:1851–1855. doi:10.1016/j.foodcont.2011.04.025
Kotzekidou P, Giannakidis P, Boulamatsis A (2008) Antimicrobial activity of some plant extracts and essential oils against foodborne pathogens in vitro and on the fate of inoculated pathogens in chocolate. LWT Food sci Technol 41:119–127. doi:10.1016/j.lwt.2007.01.016
Lima CF, Carvalho F, Fernandes E, Bastos ML, Santos-Gomes PC, Fernandes-Ferreira M, Pereira-Wilson C (2004) Evaluation of toxic/protective effects of the essential oil of Salvia officinalis on freshly isolated rat hepatocytes. Toxicol In Vitro 18:457–465. doi:10.1016/j.tiv.2004.01.001
Mathlouthi N, Bouzaienne T, Oueslati I, Recoquillay F, Hamdi M, Urdaci M, Bergaoui R (2015) Use of rosemary, oregano, and a commercial blend of essential oils in broiler chickens: in vitro antimicrobial activities and effects on growth performance. J Anim Sci 90:813–823. doi:10.2527/jas.2010-3646
Mejlholm O, Dalgaard P (2002) Antimicrobial effect of essential oils on the seafood spoilage micro-organism Photobacterium phosphoreum in liquid media and fish products. Lett Appl Microbiol 34:27–31
Miladi H, Mili D, Slama RB et al (2016) Antibiofilm formation and anti-adhesive property of three mediterranean essential oils against a foodborne pathogen Salmonella strain. Microb Pathog 93:22–31. doi:10.1016/j.micpath.2016.01.017
Mith H, Duré R, Delcenserie V, Zhiri A, Daube G, Clinquart A (2014) Antimicrobial activities of commercial essential oils and their components against food-borne pathogens and food spoilage bacteria. Food Sci Nutr 2:403–416. doi:10.1002/fsn3.116
Moghimi R, Ghaderi L, Rafati H, Aliahmadi A, McClements DJ (2016) Superior antibacterial activity of nanoemulsion of Thymus daenensis essential oil against E. coli. Food Chem 194:410–415. doi:10.1016/j.foodchem.2015.07.139
Ölmez H, Kretzschmar U (2009) Potential alternative disinfection methods for organic fresh-cut industry for minimizing water consumption and environmental impact. LWT Food sci Technol 42:686–693. doi:10.1016/j.lwt.2008.08.001
Oussalah M, Caillet S, Saucier L, Lacroix M (2006) Antimicrobial effects of selected plant essential oils on the growth of a Pseudomonas putida strain isolated from meat. Meat Sci 73:236–244. doi:10.1016/j.meatsci.2005.11.019
Pinto E, Salgueiro LR, Cavaleiro C, Palmeira A, Gonçalves MJ (2007) In vitro susceptibility of some species of yeasts and filamentous fungi to essential oils of Salvia officinalis. Ind Crops Prod 26:135–141. doi:10.1016/j.indcrop.2007.02.004
Pirie DG, Clayson DHF (1964) Some causes of unreliability of essential oils as microbial inhibitor in foods. In: Proceeding of international symposium of food microbiol (4th) Goteberg, Goteborg, Sweden, pp 145–150
Radaelli M, Silva P, Weidlich L, Hoehneb L, Flach A, Costa LAMA, Ethur EM (2016) Antimicrobial activities of six essential oils commonly used as condiments in Brazil against Clostridium perfringens. Braz J Microbiol 47:424–430. doi:10.1016/j.bjm.2015.10.001
Rojas-Graü MA, Garner E, Martin-Belloso O (2011) The fresh-cut fruit and vegetables industry cuurent situation and market trends. In: Martin-Belloso O, Soliva-Fortuny R (eds) Advances in fresh-cut fruits and vegetables processing. CRC Press, Boca Raton, pp 1–11
Rožman T, Jeršek B (2009) Antimicrobial activity of rosemary extracts (Rosmarinus officinalis L.) against different species of Listeria. Acta Agric Slov 93:51–58. doi:10.2478/v10014-009-0007-z
Sahin F, Güllüce M, Daferera D, Sokmen A, Sokmen M, Polissiou M, Agar G, Ozer H (2004) Biological activities of the essential oils and methanol extract of Origanum vulgare ssp. vulgare in the Eastern Anatolia region of Turkey. Food Control 15:549–557. doi:10.1016/j.foodcont.2003.08.009
Santos MI (2009) Estimativa da flora microbiana e eventuais patogénicos em saladas minimamente processadas (MP) prontas para consumo (Dissertação de Mestrado). Instituto Superior de Ciências da Saúde Egas Moniz, Portugal
Santos MI, Cavaco A, Gouveia J, Novais MR, Nogueira PJ, Pedroso L, Ferreira MASS (2012) Evaluation of minimally processed salads commercialized in Portugal. Food Control 23:275–281. doi:10.1016/j.foodcont.2011.06.022
Souza LI, Stamford TLM, Lima EO, Trajano VN (2007) Effectiveness of Origanum vulgare L. essential oil to inhibit the growth of food spoiling yeasts. Food Control 18:409–413. doi:10.1016/j.foodcont.2005.11.008
Uçak I, Ozogul Y, Durmus M (2011) The effects of rosemary extract combination with vacuum packing on the quality changes of Atlantic mackerel fish burgers. Int J Food Sci Technol 46:1157–1163. doi:10.1111/j.1365-2621.2011.02610.x
Vasudeva P, Vasudeva N (2015) Origanum majorama L-Phyto-pharmacological review. Indian J Nat Prod Resour 6:261–267. http://nopr.niscair.res.in/handle/123456789/33655. Accessed 8 April 2016
Acknowledgements
The authors would like to thank Dr. Alexandra Carreira and Cristina Pintado for the yeast and bacteria strains used and Polarome International, USA for kindly providing the EO. This work was supported by national funds from Fundação para a Ciência e a Tecnologia through the research unit UID/AGR/04129/2013 (LEAF).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All the authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Santos, M.I.S., Martins, S.R., Veríssimo, C.S.C. et al. Essential oils as antibacterial agents against food-borne pathogens: Are they really as useful as they are claimed to be?. J Food Sci Technol 54, 4344–4352 (2017). https://doi.org/10.1007/s13197-017-2905-0
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-017-2905-0