Volume 24, Issue 3 (12-2025)
TB 2025, 24(3): 119-131 |
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Research code: ۱۴۰۳۰۸۰۸۶۷۷۳
Ethics code: IR.UMSHA.REC.1403.545
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Arab M, Vahedi B, Ghasemzadeh-Mohammadi V, Alizadeh Salmani B, Asghari B, Rezae A. Investigating the Antibacterial Effect of a Combination of Essential Oils of the Plants in Mertus, Artemisia and Green Tea Extract on Listeria Monocytogenes, Staphylococcus Aureus and Escherichia Coli Using the Checker Board Method. TB 2025; 24 (3) :119-131
URL: http://tbj.ssu.ac.ir/article-1-3770-en.html
URL: http://tbj.ssu.ac.ir/article-1-3770-en.html
Masoumeh Arab * 
, Behnam Vahedi , Vahid Ghasemzadeh-Mohammadi , Behnam Alizadeh Salmani , Babak Asghari , Atefeh Rezae
, Behnam Vahedi , Vahid Ghasemzadeh-Mohammadi , Behnam Alizadeh Salmani , Babak Asghari , Atefeh Rezae
Shahid Sadoughi University of Medical Sciences , arab.sepideh@gmail.com
Keywords: Artemisia Absinthium, Myrtus Communis, Green Tea Extract, Staphylococcus Aureus, Listeria Monocytogenes, Escherichia Coli, Checker Board Method
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Investigating the Antibacterial Effect of a Combination of Essential Oils of the Plants in Mertus, Artemisia and Green Tea Extract on Listeria Monocytogenes, Staphylococcus Aureus and Escherichia Coli Using the Checker Board Method
Behnam Vahedi (MS)1, Vahid Ghasemzadeh-Mohammadi (Ph.D.)2, Behnam Alizadeh Salmani(M.Sc.)3, Masoumeh Arab (Ph.D.)4, Babak Asghari (Ph.D.)5, Atefeh Rezae (Ph.D.)6
1.Master's student, Department of Nutrition and Food Hygiene, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
2.Assistant professor, Department of Nutrition and Food Hygiene, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
3.Master's degree, Department of Food Sciences and Technology, School of Public Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
4.Corresponding author:Assistant professor, Department of Food Sciences and Technology, School of Public Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
Email: arab.sepideh@gmail.com Tel: 09112571419
5.Assistant professor, Department of Microbiology, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
6.Ph.D.student, Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Abstract
Introduction: Consumer awareness of the health hazards of synthetic preservatives in food has led to an increase in studies on natural preservatives. Essential oils of Artemisia(Artemisia absinthium L.) essential oil of Myrtus(Myrtus communis L.) and green tea extract are compounds that have the potential to be used in food as natural preservatives.
Methods: The antimicrobial and interaction effects of Artemisia and Myrtus essential oil and green tea extract were evaluated against three foodborne pathogens Listeria monocytogenes, Staphylococcus aureus and Escherichia colie. The minimum inhibitory concentration (MIC) was determined by phenotypic method and the antimicrobial effect was determined by checkerboard assay. Tests were repeated three times.
Results: MIC assay of Artemisia essential oil showed values of 5/12 μg/mL for Listeria monocytogenes and Escherichia colie and 25 μg/mL for Staphylococcus aureus. The MIC of Myrtus essential oil was 25 μg/mL for Listeria monocytogenes and Staphylococcus aureus and 125/3 μg/mL for Escherichia coli. Also, the MIC of green tea extract was 50 μg/mL for Listeria monocytogenes and Escherichia colie. Furthermore, fractional antibacterial combination profile (FICP) showed antagonistic interaction (antagonistic effect) and synergistic effect (synergistic effect) between the three agents against Escherichia coli and Listeria monocytogenes, while no significant interaction (indifference) was observed for Staphylococcus aureus and Escherichia coli.
Conclusion: These findings demonstrate the different antimicrobial potential of extracts derived from these three plants with significant contrast when combined with Escherichia coli, indicating caution in formulating multicomponent natural preservatives for this pathogen. The lack of synergistic or additive effects against Staphylococcus aureus emphasizes the importance of targeted selection and compatibility testing of plant antimicrobials for effective food safety interventions.
Key words: Artemisia Absinthium, Myrtus Communis, Green Tea Extract, Staphylococcus Aureus, Listeria Monocytogenes, Escherichia Coli, Checker Board Method
Conflict of interest: The authors declared no conflict of interest.
References
1-Hashemi M, Salayani M, Afshari A & et al. The global burden of viral food-borne diseases: a systematic review. Current pharmaceutical biotechnology. 2023;24(13):1657-72.
2-Tariq S, Wani S, Rasool W & et al. A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant microbial pathogens. Microbial pathogenesis. 2019;134:103580.
3-Osek J, Lachtara B, Wieczorek K. Listeria monocytogenes–how this pathogen survives in food-production environments? Frontiers in microbiology. 2022;13:866462.
4-Saraiva C, Silva AC, García-Díez J & et al. Antimicrobial activity of Myrtus communis L. and Rosmarinus officinalis L. essential oils against Listeria monocytogenes in cheese. Foods. 2021;10(5):1106.
5-Barlaam A, Parisi A, Spinelli E & et al. Global emergence of colistin-resistant Escherichia coli in food chains and associated food safety implications: a review. Journal of food protection. 2019;82(8):1440-8.
6-Basavaraju M, Gunashree B. Escherichia coli: an overview of main characteristics. Escherichia coli-old and new insights. 2022:1-21.
7-Munekata PE, Pateiro M, Rodríguez-Lázaro D & et al. The role of essential oils against pathogenic Escherichia coli in food products. Microorganisms. 2020;8(6):924.
8-Elbehiry A, Marzouk E, Alzaben F & et al. Emerging Technologies and Integrated Strategies for Microbial Detection and Control in Fresh Produce. Microorganisms. 2025;13(7):1447.
9-Bisht D, Kumar D, Kumar D & et al. Phytochemistry and pharmacological activity of the genus artemisia. Archives of Pharmacal Research. 2021;44(5):439-74.
10-de Sousa DP, Damasceno ROS, Amorati R & et al. Essential oils: Chemistry and pharmacological activities. Biomolecules. 2023;13(7):1144.
11-Giampieri F, Cianciosi D, Forbes Hernández TY. Myrtle (Myrtus communis L.) berries, seeds, leaves, and essential oils: New undiscovered sources of natural compounds with promising health benefits. Food Frontiers. 2020;1(3):276-95.
12-György É, Laslo É, Csató E. Antibacterial activity of plant extracts against isolated from ready-to-eat salads. Acta Universitatis Sapientiae, Alimentaria. 2020;13(1):131-43.
13-Kim W-S, Choi WJ, Lee S & et al. Anti-inflammatory, antioxidant and antimicrobial effects of artemisinin extracts from Artemisia annua L. Korean Journal of Physiology & Pharmacology. 2015;19(1):21-7.
14-Kochman J, Jakubczyk K, Antoniewicz J & et al. Health benefits and chemical composition of matcha green tea: A review. Molecules. 2020;26(1):85.
15-Lencova S, Zdenkova K, Demnerova K & et al. Antibacterial and antibiofilm effect of natural substances and their mixtures over Listeria monocytogenes, Staphylococcus aureus and Escherichia coli. Lwt. 2022;154:112777.
16-Hennia A, Nemmiche S, Dandlen S & et al. Myrtus communis essential oils: insecticidal, antioxidant and antimicrobial activities: a review. Journal of Essential Oil Research. 2019;31(6):487-545.
17-Gan C, Langa E, Valenzuela A & et al. Synergistic activity of thymol with commercial antibiotics against critical and high WHO priority pathogenic bacteria. Plants. 2023;12(9):1868.
18-Franconi I, Lupetti A. In Vitro Susceptibility Tests in the Context of Antifungal Resistance: Beyond Minimum Inhibitory Concentration in Candida spp. Journal of fungi (Basel, Switzerland). 2023;9(12).
19-Sartini S, Djide MN, Amir MN & et al. Phenolic-rich green tea extract increases the antibacterial activity of amoxicillin against Staphylococcus aureus by in vitro and ex vivo studies. J Pharm Pharmacogn Res. 2020;8(6):491-500.
20-Răzvan PD, Cristinela ID, Rodica B. Comparative Quantitative Analysis of some Classes of Bioactive Compounds in six Green Tea Types Available on The Romanian Market. 2020.
21-Liu S, Zhang Q, Li H & et al. Comparative Assessment of the Antibacterial Efficacies and Mechanisms of Different Tea Extracts. Foods. 2022;11(4).
22-José da Costa G, dos Santos RM, Cerávolo IP & et al. Green Tea (Camellia sinensis) Extract is Effective against Biofilms of Staphylococcus aureus and Pseudomonas aeruginosa, and Interferes on the Activity of Antimicrobial Drugs. Current Functional Foods. 2023;1(2):E190423216032.
23-Aleksic V, Knezevic P. Antimicrobial and antioxidative activity of extracts and essential oils of Myrtus communis L. Microbiological research. 2014;169(4):240-54.
24-Moo C-L, Osman MA, Yang S-K & et al. Antimicrobial activity and mode of action of 1,8-cineol against carbapenemase-producing Klebsiella pneumoniae. Scientific Reports. 2021;11(1):20824.
25-Ouedrhiri W, Mechchate H, Moja S & et al. Optimized antibacterial effects in a designed mixture of essential oils of Myrtus communis, Artemisia herba-alba and Thymus serpyllum for wide range of applications. Foods. 2022;11(1):132.
26-Barhouchi B, Menacer R, Bouchkioua S & et al. Compounds from myrtle flowers as antibacterial agents and SARS-CoV-2 inhibitors: In-vitro and molecular docking studies. Arabian journal of chemistry. 2023;16(8):104939.
Behnam Vahedi (MS)1, Vahid Ghasemzadeh-Mohammadi (Ph.D.)2, Behnam Alizadeh Salmani(M.Sc.)3, Masoumeh Arab (Ph.D.)4, Babak Asghari (Ph.D.)5, Atefeh Rezae (Ph.D.)6
1.Master's student, Department of Nutrition and Food Hygiene, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
2.Assistant professor, Department of Nutrition and Food Hygiene, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
3.Master's degree, Department of Food Sciences and Technology, School of Public Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
4.Corresponding author:Assistant professor, Department of Food Sciences and Technology, School of Public Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
Email: arab.sepideh@gmail.com Tel: 09112571419
5.Assistant professor, Department of Microbiology, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
6.Ph.D.student, Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Abstract
Introduction: Consumer awareness of the health hazards of synthetic preservatives in food has led to an increase in studies on natural preservatives. Essential oils of Artemisia(Artemisia absinthium L.) essential oil of Myrtus(Myrtus communis L.) and green tea extract are compounds that have the potential to be used in food as natural preservatives.
Methods: The antimicrobial and interaction effects of Artemisia and Myrtus essential oil and green tea extract were evaluated against three foodborne pathogens Listeria monocytogenes, Staphylococcus aureus and Escherichia colie. The minimum inhibitory concentration (MIC) was determined by phenotypic method and the antimicrobial effect was determined by checkerboard assay. Tests were repeated three times.
Results: MIC assay of Artemisia essential oil showed values of 5/12 μg/mL for Listeria monocytogenes and Escherichia colie and 25 μg/mL for Staphylococcus aureus. The MIC of Myrtus essential oil was 25 μg/mL for Listeria monocytogenes and Staphylococcus aureus and 125/3 μg/mL for Escherichia coli. Also, the MIC of green tea extract was 50 μg/mL for Listeria monocytogenes and Escherichia colie. Furthermore, fractional antibacterial combination profile (FICP) showed antagonistic interaction (antagonistic effect) and synergistic effect (synergistic effect) between the three agents against Escherichia coli and Listeria monocytogenes, while no significant interaction (indifference) was observed for Staphylococcus aureus and Escherichia coli.
Conclusion: These findings demonstrate the different antimicrobial potential of extracts derived from these three plants with significant contrast when combined with Escherichia coli, indicating caution in formulating multicomponent natural preservatives for this pathogen. The lack of synergistic or additive effects against Staphylococcus aureus emphasizes the importance of targeted selection and compatibility testing of plant antimicrobials for effective food safety interventions.
Key words: Artemisia Absinthium, Myrtus Communis, Green Tea Extract, Staphylococcus Aureus, Listeria Monocytogenes, Escherichia Coli, Checker Board Method
Conflict of interest: The authors declared no conflict of interest.
References
1-Hashemi M, Salayani M, Afshari A & et al. The global burden of viral food-borne diseases: a systematic review. Current pharmaceutical biotechnology. 2023;24(13):1657-72.
2-Tariq S, Wani S, Rasool W & et al. A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant microbial pathogens. Microbial pathogenesis. 2019;134:103580.
3-Osek J, Lachtara B, Wieczorek K. Listeria monocytogenes–how this pathogen survives in food-production environments? Frontiers in microbiology. 2022;13:866462.
4-Saraiva C, Silva AC, García-Díez J & et al. Antimicrobial activity of Myrtus communis L. and Rosmarinus officinalis L. essential oils against Listeria monocytogenes in cheese. Foods. 2021;10(5):1106.
5-Barlaam A, Parisi A, Spinelli E & et al. Global emergence of colistin-resistant Escherichia coli in food chains and associated food safety implications: a review. Journal of food protection. 2019;82(8):1440-8.
6-Basavaraju M, Gunashree B. Escherichia coli: an overview of main characteristics. Escherichia coli-old and new insights. 2022:1-21.
7-Munekata PE, Pateiro M, Rodríguez-Lázaro D & et al. The role of essential oils against pathogenic Escherichia coli in food products. Microorganisms. 2020;8(6):924.
8-Elbehiry A, Marzouk E, Alzaben F & et al. Emerging Technologies and Integrated Strategies for Microbial Detection and Control in Fresh Produce. Microorganisms. 2025;13(7):1447.
9-Bisht D, Kumar D, Kumar D & et al. Phytochemistry and pharmacological activity of the genus artemisia. Archives of Pharmacal Research. 2021;44(5):439-74.
10-de Sousa DP, Damasceno ROS, Amorati R & et al. Essential oils: Chemistry and pharmacological activities. Biomolecules. 2023;13(7):1144.
11-Giampieri F, Cianciosi D, Forbes Hernández TY. Myrtle (Myrtus communis L.) berries, seeds, leaves, and essential oils: New undiscovered sources of natural compounds with promising health benefits. Food Frontiers. 2020;1(3):276-95.
12-György É, Laslo É, Csató E. Antibacterial activity of plant extracts against isolated from ready-to-eat salads. Acta Universitatis Sapientiae, Alimentaria. 2020;13(1):131-43.
13-Kim W-S, Choi WJ, Lee S & et al. Anti-inflammatory, antioxidant and antimicrobial effects of artemisinin extracts from Artemisia annua L. Korean Journal of Physiology & Pharmacology. 2015;19(1):21-7.
14-Kochman J, Jakubczyk K, Antoniewicz J & et al. Health benefits and chemical composition of matcha green tea: A review. Molecules. 2020;26(1):85.
15-Lencova S, Zdenkova K, Demnerova K & et al. Antibacterial and antibiofilm effect of natural substances and their mixtures over Listeria monocytogenes, Staphylococcus aureus and Escherichia coli. Lwt. 2022;154:112777.
16-Hennia A, Nemmiche S, Dandlen S & et al. Myrtus communis essential oils: insecticidal, antioxidant and antimicrobial activities: a review. Journal of Essential Oil Research. 2019;31(6):487-545.
17-Gan C, Langa E, Valenzuela A & et al. Synergistic activity of thymol with commercial antibiotics against critical and high WHO priority pathogenic bacteria. Plants. 2023;12(9):1868.
18-Franconi I, Lupetti A. In Vitro Susceptibility Tests in the Context of Antifungal Resistance: Beyond Minimum Inhibitory Concentration in Candida spp. Journal of fungi (Basel, Switzerland). 2023;9(12).
19-Sartini S, Djide MN, Amir MN & et al. Phenolic-rich green tea extract increases the antibacterial activity of amoxicillin against Staphylococcus aureus by in vitro and ex vivo studies. J Pharm Pharmacogn Res. 2020;8(6):491-500.
20-Răzvan PD, Cristinela ID, Rodica B. Comparative Quantitative Analysis of some Classes of Bioactive Compounds in six Green Tea Types Available on The Romanian Market. 2020.
21-Liu S, Zhang Q, Li H & et al. Comparative Assessment of the Antibacterial Efficacies and Mechanisms of Different Tea Extracts. Foods. 2022;11(4).
22-José da Costa G, dos Santos RM, Cerávolo IP & et al. Green Tea (Camellia sinensis) Extract is Effective against Biofilms of Staphylococcus aureus and Pseudomonas aeruginosa, and Interferes on the Activity of Antimicrobial Drugs. Current Functional Foods. 2023;1(2):E190423216032.
23-Aleksic V, Knezevic P. Antimicrobial and antioxidative activity of extracts and essential oils of Myrtus communis L. Microbiological research. 2014;169(4):240-54.
24-Moo C-L, Osman MA, Yang S-K & et al. Antimicrobial activity and mode of action of 1,8-cineol against carbapenemase-producing Klebsiella pneumoniae. Scientific Reports. 2021;11(1):20824.
25-Ouedrhiri W, Mechchate H, Moja S & et al. Optimized antibacterial effects in a designed mixture of essential oils of Myrtus communis, Artemisia herba-alba and Thymus serpyllum for wide range of applications. Foods. 2022;11(1):132.
26-Barhouchi B, Menacer R, Bouchkioua S & et al. Compounds from myrtle flowers as antibacterial agents and SARS-CoV-2 inhibitors: In-vitro and molecular docking studies. Arabian journal of chemistry. 2023;16(8):104939.
Type of Study: Research |
Subject:
microbilogy
Received: 2025/05/13 | Accepted: 2025/07/21 | Published: 2025/12/31
Received: 2025/05/13 | Accepted: 2025/07/21 | Published: 2025/12/31
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