Cited by 218Essential Oils and Antimicrobial ActivityAntimicrobial agents and applicationsProbiotics and Fermented Foods

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Activity of natural antimicrobial compounds against Escherichia coli and Salmonella enterica serovar Typhimurium

Olasupo, N.A., Fitzgerald, D.J., Gasson, M.J., Narbad, A.·2003·Letters in Applied Microbiology

DOI 10.1046/j.1472-765x.2003.01427.x

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Abstract

AIMS: The objective of this study was to evaluate the inhibitory activity of several natural organic compounds alone or in combination with nisin against Escherichia coli and Salmonella Typhimurium. METHODS AND RESULTS: The minimum inhibitory concentration (MIC) of five natural organic compounds were determined, and the effect of their combinations with nisin was evaluated by the checkerboard assay using the Bioscreen C. As expected, nisin by itself showed no inhibition against either of the Gram-negative bacteria. Thymol was found to be the most effective with the lowest MIC values of 1.0 and 1.2 mmol 1-1 against Salm. Typhimurium and E. coli, respectively. After thymol, the antimicrobial order of the natural organic compounds was carvacrol > eugenol > cinnamic acid > diacetyl. However, the combination of nisin with the natural organic compounds did not result in the enhancement of their antimicrobial activities. On the contrary, combination of nisin with diacetyl against Salm. Typhimurium resulted in an antagonism of diacetyl activity. CONCLUSIONS: While the individual natural organic compounds showed inhibitory activity against the two Gram-negatives, their combinations with nisin showed no improvement of antimicrobial activity. SIGNIFICANCE AND IMPACT OF THE STUDY: This study shows the potential of the natural organic compounds to control E. coli and Salm. Typhimurium.

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Gutiérrez-Pacheco, M. M., González-Aguilar, G. A., Martínez‐Téllez, M. Á., Lizardi‐Mendoza, J., Madera-Santana, T. J., Bernal-Mercado, A. T., Vázquez-Armenta, F. J., & Ayala-Zavala, J. F. (2018) · Food Control · doi:10.1016/j.foodcont.2018.02.007 · Cited by 61
Effects of Common Forage Phenolic Acids on Escherichia coli O157:H7 Viability in Bovine Feces
Wells, J. E., Berry, E. D., & Varel, V. H. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.7974-7979.2005 · Cited by 58
“Recognizing the differences with the time on the diet, the adaptation of ruminants to forages, and the ability of plant phenolic acids to affect pathogens in in vitro studies (13, 20, 28, 39) led us to analyze the effects of phenolic acids in bovine feces.”
Background
The effects of methylcellulose coating containing carvacrol or menthol on the physicochemical, mechanical, and antimicrobial activity of polyethylene films
Jahdkaran, E., Hosseini, S. E., Nafchi, A. M., & Nouri, L. (2021) · Food Science & Nutrition · doi:10.1002/fsn3.2240 · Cited by 56
Antibacterial activity of pullulan films containing thymol
Gniewosz, M., & Synowiec, A. (2011) · Flavour and Fragrance Journal · doi:10.1002/ffj.2063 · Cited by 58
Gastrointestinal Absorption and Urinary Excretion of trans-Cinnamic and p-Coumaric Acids in Rats
Garrait, G., Jarrige, J.-F., Blanquet, S., Beyssac, E., Cardot, J., & Alric, M. (2006) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf053169a · Cited by 54
Short communication: Combined antimicrobial activity of reuterin and diacetyl against foodborne pathogens
Langa, S., Martín‐Cabrejas, I., Montiel, R., Landete, J. M., Médina, M., & Arqués, J. L. (2014) · Journal of Dairy Science · doi:10.3168/jds.2014-8306 · Cited by 53
“A pH of 5.0 or less is common in many cheese varieties and fermented milks, and antimicrobial activity of diacetyl at concentrations ranging between 300 and 10,000 mg/ kg against E. coli, Salmonella, and L. monocytogenes has been reported (Jay, 1982; Olasupo et al., 2003; O’Bryan et al., 2009).”
Influential
Comparative analysis of selected methods for the assessment of antimicrobial and membrane-permeabilizing activity: a case study for lactoferricin derived peptides
Sánchez-Gómez, S., Lamata, M., Leiva, J., Blondelle, S. E., Jerala, R., Andrä, J., Brandenburg, K., Lohner, K., Moriyón, I., & de Tejada, G. M. (2008) · BMC Microbiology · doi:10.1186/1471-2180-8-196 · Cited by 50
“Moreover, for the calculation of the MIC by broth microdilution-based assays, some investigators emphasize the importance of using microplates made of polypropylene [18-20], whereas others perform their assays on automated turbidimetric systems [21-23], the latter being preferred by those dealing with high-throughput…”
Inhibitory activity of natural antimicrobial compounds alone or in combination with nisin againstEnterobacter sakazakii
Lee, S.-Y., & Jin, H.-H. (2008) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2008.02432.x · Cited by 52
“Furthermore, other researchers reported that there was no synergistic effect in the combination of nisin with organic compounds against E. coli and S. Typhimurium (Olasupo et al. 2003).”
BackgroundInfluential
Nisin A and Polymyxin B as Synergistic Inhibitors of Gram-positive and Gram-negative Bacteria
Naghmouchi, K., Drider, D., Baah, J., & Teather, R. M. (2010) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-009-9033-8 · Cited by 50
“Olasupo et al. [ 18 ] evaluated the inhibitory activity of nisin alone or in combination with several natural organic compounds against E. coli and Salmonella enterica serovar Typhimurium and found that no combination enhanced antimicrobial activity.”
Background
Antimicrobial activity of Lippia gracilis essential oils on the plant pathogen Xanthomonas campestris pv. campestris and their effect on membrane integrity
da Silva, R. S., de Oliveira, M. M. G., de Melo, J. O., Blank, A. F., Corrêa, C. B., Scher, R., & Fernandes, R. P. M. (2019) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2019.06.014 · Cited by 50
The beneficial role of plant based thymol in food packaging application: A comprehensive review
Sivaram, S., Somanathan, H., Kumaresan, S. M., & Sundaram, M. (2022) · Applied Food Research · doi:10.1016/j.afres.2022.100214 · Cited by 49
Analysis of the essential oil components from different Carum copticumL. samples from Iran
Zarshenas, M. M., Samani, S. M., Petramfar, P., & Moein, M. (2013) · Pharmacognosy Research · doi:10.4103/0974-8490.122920 · Cited by 49
“Many investigations have explored the antimicrobial and antioxidant properties of this component.[29,30] Thymol also possesses anti-infl ammatory,[31] analgesic and local anesthetic[32] effects.”
Background
Insight into the antibacterial property of chitosan nanoparticles against Escherichia coli and Salmonella Typhimurium and their application as vegetable wash disinfectant
Paomephan, P., Assavanig, A., Chaturongakul, S., Cady, N. C., Bergkvist, M., & Niamsiri, N. (2017) · Food Control · doi:10.1016/j.foodcont.2017.09.021 · Cited by 48
Short Linear Cationic Antimicrobial Peptides: Screening, Optimizing, and Prediction
Hilpert, K., Fjell, C. D., & Cherkasov, A. R. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-419-3_8 · Cited by 46
The application of thymol-loaded chitosan nanoparticles to control the biodeterioration of cultural heritage sites
Wang, X., Hu, Y., Zhang, Z., & Zhang, B. (2021) · Journal of Cultural Heritage · doi:10.1016/j.culher.2021.12.002 · Cited by 46
Chemical Composition and Antimicrobial Activity of the Essential Oil of Algerian Phlomis bovei De Noé subsp. bovei
Liolios, C. C., Laouer, H., Boulaacheb, N., Gortzi, O., & Chinou, İ. (2007) · Molecules · doi:10.3390/12040772 · Cited by 46
“bovei can be attributed, to a considerable degree, to the presence of germacrene D and thymol, which are well known to posses strong antimicrobial activity [13-15].”
Antibacterial activity of jalapeño pepper (Capsicum annuum var. annuum) extract fractions against select foodborne pathogens
Bacon, K., Boyer, R. R., Denbow, C. J., O’Keefe, S. F., Neilson, A. P., & Williams, R. C. (2017) · Food Science & Nutrition · doi:10.1002/fsn3.453 · Cited by 45
Rational Engineering of Phenylalanine Accumulation in Pseudomonas taiwanensis to Enable High-Yield Production of Trans-Cinnamate
Otto, M., Wynands, B., Lenzen, C., Filbig, M., Blank, L. M., & Wierckx, N. J. P. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00312 · Cited by 45
Plants: A natural solution to enhance raw milk cheese preservation?
Dupas, C., Métoyer, B., El‐Hatmi, H., Adt, I., Mahgoub, S. A., & Dumas, E. (2019) · Food Research International · doi:10.1016/j.foodres.2019.108883 · Cited by 50
Untangling the bioactive properties of therapeutic deep eutectic solvents based on natural terpenes
Silva, E., Oliveira, F., Silva, J. M., Reis, R. L., & Duarte, A. R. C. (2021) · Current Research in Chemical Biology · doi:10.1016/j.crchbi.2021.100003 · Cited by 44
Synergistic Effects and Physiological Responses of Selected Bacterial Isolates from Animal Feed to Four Natural Antimicrobials and Two Antibiotics
Zhang, D., Hu, H., Rao, Q., & Zhao, Z. (2011) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2010.0817 · Cited by 43
“It has been well documented that essential oils or their active components from wild plants’ natural defense systems can act as effective antimicrobials (Ultee et al. , 1999; Olasupo et al. , 2003; Li et al. , 2010).”
Sodium alginate edible coating containing Ferulago angulata (Schlecht.) Boiss essential oil, nisin, and NaCl: Its impact on microbial, chemical, and sensorial properties of refrigerated chicken breast
Panahi, Z., & Mohsenzadeh, M. (2022) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2022.109883 · Cited by 42
Thymol Disrupts Cell Homeostasis and Inhibits the Growth of Staphylococcus aureus
Li, Q., Huang, K. X., Pan, S., Su, C., Bi, J., & Lu, X. (2022) · Contrast Media & Molecular Imaging · doi:10.1155/2022/8743096 · Cited by 41
Inactivation of Salmonella enterica serovar Typhimurium and Quality Maintenance of Cherry Tomatoes Treated with Gaseous Essential Oils
Yun, J., Fan, X., & Li, X. (2013) · Journal of Food Science · doi:10.1111/1750-3841.12052 · Cited by 40
Pharmacological activities and medicinal properties of endemic Moroccan medicinal plant Origanum compactum (Benth) and their main compounds
Bouyahya, A., Guaouguaou, F., Dakka, N., & Bakri, Y. (2017) · Asian Pacific Journal of Tropical Disease · doi:10.12980/apjtd.7.2017d7-31 · Cited by 39
“The antibacterial effects of thymol have been evaluated by several studies[95-100] against E.”
Background
ANTIMICROBIALS USED IN ACTIVE PACKAGING FILMS
Dıblan, S., & Kaya, S. (2018) · Food and Health · doi:10.3153/jfhs18007 · Cited by 39
Antibacterial Activities of Thymol, Eugenol and Nisin Against Some Food Spoilage Bacteria
Tippayatum, P., & Chonhenchob, V. (2007) · Agriculture and Natural Resources · Cited by 38
Antibacterial activity of essential oils: potential applications in food
Burt, S. A. (2002) · Utrecht University Repository (Utrecht University) · Cited by 38
The Herbal Compound Thymol Protects Mice From Lethal Infection by Salmonella Typhimurium
Zhang, Y., Liu, Y., Qiu, J., Luo, Z., & Deng, X. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01022 · Cited by 37
“Thymol has been reported to have antimicrobial against S. Typhimurium, but the MIC reported by different studies varied greatly, ranging from 150µg/ml (1.0mM) (Olasupo et al., 2003) to 750µg/ml (5.0mM) (Chauhan and Kang, 2014).”
Background
Influence of Cinnamon and Clove Essential Oils on the D - and z-Values of Escherichia coli O157:H7 in Apple Cider
Knight, K. P., & McKellar, R. C. (2007) · Journal of Food Protection · doi:10.4315/0362-028x-70.9.2089 · Cited by 39
The inhibitory effect of natural bioactives on the growth of pathogenic bacteria
Kim, J., & Kim, Y. (2007) · Nutrition Research and Practice · doi:10.4162/nrp.2007.1.4.273 · Cited by 36
Potential To Reduce Escherichia coli Shedding in Cattle Feces by Using Sainfoin ( Onobrychis viciifolia ) Forage, Tested In Vitro and In Vivo
Berard, N., Holley, R. A., McAllister, T. A., Ominski, K., Wittenberg, K. M., Bouchard, K. S., Bouchard, J. J., & Krause, D. O. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00983-08 · Cited by 36
“Phytochemicals/tannins have antimicrobial properties against E. coli (9, 14, 28 , 40).”
Background
Enhanced synthesis and antimicrobial activities of bacteriocins produced by Mexican strains of Bacillus thuringiensis
de la Fuente‐Salcido, N. M., Alanís-Guzmán, M. G., Bideshi, D. K., Salcedo‐Hernández, R., Justo, M. B., & Barboza-Corona, J. E. (2008) · Archives of Microbiology · doi:10.1007/s00203-008-0414-2 · Cited by 36
“As such, there is growing interest in expanding the use of eVective natural antimicrobials such as thymol, carvacrol and bacteriocins as preservatives ( Olasupo et al. 2003 ).”
Background
Investigation of Antifungal Mechanisms of Thymol in the Human Fungal Pathogen, Cryptococcus neoformans
Jung, K., Chung, M., Bai, H., Chung, B.-Y., & Lee, S. (2021) · Molecules · doi:10.3390/molecules26113476 · Cited by 36
“Thymol also exhibits antibacterial activity against an array of Gram-positive and Gram-negative strains [9,10].”
Background
Thymol-Loaded Eudragit RS30D Cationic Nanoparticles-Based Hydrogels for Topical Application in Wounds: In Vitro and In Vivo Evaluation
Mohsen, A. M., Nagy, Y. I., Shehabeldine, A. M., & Okba, M. M. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics15010019 · Cited by 35
“Moreover, the antibacterial activity of thymol is also superior to those of other essential oil constituents such as carvacrol, cinnamic acid, eugenol, and diacetyl [7].”
Background
Antimicrobial Activity of Natural Agents Coated on Starch‐Based Films against Staphylococcus aureus
Kuorwel, K. K., Cran, M. J., Sonneveld, K., Miltz, J. W., & Bigger, S. W. (2011) · Journal of Food Science · doi:10.1111/j.1750-3841.2011.02344.x · Cited by 35
Antibacterial activities of plant-derived compounds and essential oils against Cronobacter strains
Berthold‐Pluta, A., Stasiak-Różańska, L., Pluta, A., & Garbowska, M. (2018) · European Food Research and Technology · doi:10.1007/s00217-018-3218-x · Cited by 35
Screening of Commercial and Pecan Shell-Extracted Liquid Smoke Agents as Natural Antimicrobials against Foodborne Pathogens
Loo, E. J. V., Babu, D., Crandall, P. G., & Ricke, S. C. (2012) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-11-543 · Cited by 35
“Different natural or organic alternative antimicrobials, such as bacteriocins, bacteriophages, and natural plant extracts such as essential oils and liquid smokes, have been studied for their antimicrobial activities against foodborne pathogens and food spoilage microorganisms (4, 10, 16, 22, 26).”
Background
In vitro antibacterial activity and volatile characterisation of organic Apis mellifera ligustica (Spinola, 1906) beeswax ethanol extracts
Felicioli, A., Cilia, G., Mancini, S., Turchi, B., Galaverna, G., Cirlini, M., Cerri, D., & Fratini, F. (2019) · Food Bioscience · doi:10.1016/j.fbio.2019.04.004 · Cited by 33
Antibacterial activity and membrane-disrupting mechanism of monocaprin against Escherichia coli and its application in apple and carrot juices
Ma, M., Zhao, J., Zeng, Z., Wan, D., Yu, P., Cheng, D., Gong, D., & Deng, S. (2020) · LWT · doi:10.1016/j.lwt.2020.109794 · Cited by 32

Authors: Olasupo, N. A., Fitzgerald, D. J., Gasson, M. J., & Narbad, A.
Affiliations: Lagos State University (NG)
Norwich Research Park (GB)
Corresponding author: Narbad, A.
ORCID: Olasupo, N.A.
Narbad, A.
Venue: Letters in Applied Microbiology
Publisher: Oxford University Press (OUP)
Published: 2003-12
Volume: 37
Issue: 6
Pages: 448-451
ISSN: 0266-8254 (ISSN-L)
1365-2673
DOI: 10.1046/j.1472-765x.2003.01427.x
OpenAlex: W1970033253
Cited by: 218
References: 22
Citations by year: 2026: 2 · 2025: 5 · 2024: 4 · 2023: 7 · 2022: 11 · 2021: 19 · 2020: 11 · 2019: 12 · 2018: 16 · 2017: 13 · 2016: 8 · 2015: 9 · 2014: 10 · 2013: 12 · 2012: 12
FWCI: 4.35
Type: journal article
Language: en
Open access: closed
Licence: doi.wiley.com/10.1002/tdm_license_1.1 (tdm, 4292 d)
Locations: Letters in Applied Microbiology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Essential Oils and Antimicrobial Activity
Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antimicrobial agents and applications
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords: natural antimicrobials, Escherichia coli, Salmonella typhimurium, nisin, thymol, carvacrol, eugenol, cinnamic acid, diacetyl, minimum inhibitory concentration, synergistic and antagonistic effects, Gram-negative bacteria, food safety
MeSH terms: Cymenes, Anti-Bacterial Agents, Cinnamates, Diacetyl, Drug Therapy, Combination, Escherichia coli, Eugenol, Microbial Sensitivity Tests, Nisin, Salmonella typhimurium, Thymol, Monoterpenes, In Vitro Techniques

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Activity of natural antimicrobial compounds against Escherichia coli and Salmonella enterica serovar Typhimurium

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