Antistaphylococcal activity of Thymus vulgaris and Origanum vulgare essential oils: time-lapse kinetics, antibiofilm activity and synergistic potential

Zorica Stojanović-Radić, Marina Dimitrijević, Ana Aleksić, Nikola Stanković

Abstract


Staphylococcus aureus is one of the most frequent human pathogens, whose high virulence and severity of chronic infections are related to their ability to produce biofilms. In the present study, antimicrobial potential of oregano and thyme essential oils on the planktonic growth of S. aureus clinical strains (isolated from nose, throat and wound), as well as the effect of the oils on the biofilm production, compared with conventional antibiotic streptomycin were investigated. In addition, time-lapse kinetics and combinations of individual oils with streptomycin were investigated for synergism against the selected staphylococcal strains. The results showed high potential of both oils where minimal inhibitory values ranged between 0.078 and 2.50 mg/ml, while biofilms were reduced up to 96%. In the case of biofilms, the reverse concentration dependency has been observed. Time-lapse kinetics showed recovery of some strains after 4 h of contact with the oils, but these strains demonstrated significantly reduced growth in comparison to the control. All mentioned assays showed slightly higher efficacy of oregano essential oil. Calculated FICs showed either synergistic or additive effect of all tested combinations (thyme-oregano, thyme-streptomycin, oregano-streptomycin), with the thyme-streptomycin as the most efficient one. All mentioned results point to a very high potential of both oils to be used as an adjuvant agent for control of human staphylococcal infections.


Keywords


thyme; oregano; Staphylococcus aureus; antibiofilm activity; synergism; clinical isolates

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Abdallah, F. Ben, Lagha, R., & Gaber, A. 2020: Biofilm inhibition and eradication properties of medicinal plant essential oils against methicillin-resistant Staphylococcus aureus Clinical Isolates. Pharmaceuticals, 13: 369.

Araujo, M. M. de, & Longo, P. L. 2016: Teste da ação antibacteriana in vitro de óleo essencial comercial de Origanum vulgare (orégano) diante das cepas de Escherichia coli e Staphylococcus aureus. Arquivos Do Instituto Biológico, 83: 1–7.

Ben Abdallah, F., Lagha, R., & Gaber, A. 2020: Biofilm inhibition and eradication properties of medicinal plant essential oils against methicillin-resistant Staphylococcus aureus clinical isolates. Pharmaceuticals, 13(11): 1–15.

Benabed, K. H., Gourine, N., Ouinten, M., Yousfi, M., Bombarda, I., & Yousfi, M. 2016: Chemical composition, antioxidant and antimicrobial activities of the essential oils of three Algerian Lamiaceae species. Current Nutrition and Food Science, 13(2): 97–109.

Bilge, N., Vatansever, L., & Duman, B. 2010: Effect of oregano essential oil on biofilms formed by staphylococci and Escherichia coli. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16 (Suppl-A): 22–29.

Boskovic, M., Zdravkovic, N., Ivanovic, J., Janjic, J., Djordjevic, J., Starcevic, M., & Baltic, M. Z. 2015: Antimicrobial activity of thyme (Tymus vulgaris) and oregano (Origanum vulgare) essential oils against some food-borne microorganisms. Procedia Food Science, 5: 18–21.

de Carvalho, R. J., de Souza, G. T., Honório, V. G., de Sousa, J. P., da Conceição, M. L., Maganani, M., de Souza, E. L. 2015: Comparative inhibitory effects of Thymus vulgaris L. essential oil against Staphylococcus aureus, Listeria monocytogenes and mesophilic starter co-culture in cheese-mimicking models. Food Microbiology, 52: 59–65.

de Souza, E. L., de Barros, J. C., da Conceição, M. L., Neto, N. J. G., & da Costa, A. C. V. 2009: Combined application of Origanum vulgare l. essential oil and acetic acid for controlling the growth of Staphylococcus aureus in foods. Brazilian Journal of Microbiology, 40(2): 387–393.

Evangelista-Martínez, Z., Reyes-Vázquez, N., & Rodríguez-Buenfil, I. 2018: Antimicrobial evaluation of plant essential oils against pathogenic microorganisms: In vitro study of oregano oil combined with conventional food preservatives. Acta Universitaria, 28(4): 10–18.

Fani, M., & Kohanteb, J. 2017: In Vitro antimicrobial activity of Thymus vulgaris essential oil against major oral pathogens. Journal of Evidence-Based Complementary and Alternative Medicine, 22(4): 660–666.

García-Díez, J., Alheiro, J., Pinto, A. L., Falco, V., Fraqueza, M. J., & Patarata, L. 2017: Synergistic activity of essential oils from herbs and spices used on meat products against food borne pathogens. Natural Product Communications, 12(2): 281–286.

Gedikoğlu, A., Sökmen, M., & Çivit, A. 2019: Evaluation of Thymus vulgaris and Thymbra spicata essential oils and plant extracts for chemical composition, antioxidant, and antimicrobial properties. Food Science and Nutrition, 7(5): 1704–1714.

Kavanaugh, N. L., & Ribbeck, K. 2012: Selected antimicrobial essential oils eradicate Pseudomonas spp. and Staphylococcus aureus biofilms. Applied and Environmental Microbiology, 78(11): 4057–4061.

Kazemi, M., Mousavi, E., & Bandrez, N. 2012: Chemical compositions and antibacterial activity of the essential oils of Thymus vulgaris and Tanacetum perthenium. Research Journal of Soil Biology, 4(2): 21–31.

Kon, K., & Rai, M. 2012: Antibacterial activity of Thymus vulgaris essential oil alone and in combination with other essential oils. Nusantara Bioscience, 4(2): 50–56.

Lu, M., Dai, T., Murray, C. K., Wu M. X. 2018. Bactericidal property of Oregano Oil against multidrug-resistant clinical isolates. Frontiers in Microbiology, 9: 2329.

Lv, F., H. Liang, Q. Yuan, and C. Li. 2011. In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms. Food Research International, 44: 3057–3064.

Man, A., Santacroce, L., Jacob, R., Mare, A., & Man, L. 2019: Antimicrobial activity of six essential oils against a group of human pathogens: A comparative study. Pathogens, 8(15): 1–11.

Marques, J. de L., Volcão, L. M., Funck, G. D., Kroning, I. S., da Silva, W. P., Fiorentini, Â. M., & Ribeiro, G. A. 2015: Antimicrobial activity of essential oils of Origanum vulgare L. and Origanum majorana L. against Staphylococcus aureus isolated from poultry meat. Industrial Crops and Products, 77: 444–450.

Najem, A.H. 2020: In vitro antimicrobial and antibiofilm activity of some plant essential oils against nasal Staphylococcus aureus. Journal of Critical Reviews, 7(5): 892–898.

Nostro, A., Roccaro, A. S., Bisignano, G., Marino, A., Cannatelli, M. A., Pizzimenti, F. C., Cioni, P. L., Procopio, F., & Blanco, A. R. 2007: Effects of oregano, carvacrol and thymol on Staphylococcus aureus and Staphylococcus epidermidis biofilms. Journal of Medical Microbiology, 56: 519–523.

Özkalp, B., Sevgi, F., Özcan, M., & Özcan, M. M. 2010: The antibacterial activity of essential oil of oregano (Origanum vulgare L.). Journal of Food, Agriculture and Environment, 8(2): 272–274.

Papa, R., Garzoli, S., Vrenna, G., Sabatino, M., Sapienza, F., Relucenti, M., Donfrancesco, O., Fiscarelli, E. V., Artini, M., Selan, L., & Ragno, R. 2020: Essential oils biofilm modulation activity, chemical and machine learning analysis. Application on Staphylococcus aureus isolates from cystic fibrosis patients. International Journal of Molecular Sciences, 21(23): 1–20.

Pecarski, D., Ketin, S., Omerovic, I., Mirkovic, M., Jugovic, Z., & Biocanin, R. 2016: Chemical compositions and antimicrobial activities of oregano and thyme essential oils . Bulgarian Chemical Communications, 48 (4): 678 – 683.

Pejčić, M., Stojanović-Radić, Z., Genčić, M., Dimitrijević, M., & Radulović, N. 2020: Anti-virulence potential of basil and sage essential oils: Inhibition of biofilm formation, motility and pyocyanin production of Pseudomonas aeruginosa isolates. Food and Chemical Toxicology, 141: 111431.

Pesavento, G., Calonico, C., Bilia, A. R., Barnabei, M., Calesini, F., Addona, R., Mencarelli, L., Carmagnini, L., Di Martino, M. C., & Lo Nostro, A. 2015: Antibacterial activity of oregano, rosmarinus and thymus essential oils against Staphylococcus aureus and Listeria monocytogenes in beef meatballs. Food Control, 54: 188–199.

Pourazar Dizaji‎, S., Soleimani, N., Afrugh, P., & Saedi‎, S. 2018: In vitro antibacterial activity of Thymus vulgaris essential oil against Mycobacterium tuberculosis. Infection Epidemiology and Microbiology, 4(2): 47–51.

Prince, A. (2013). Staphylococcus aureus infection in the respiratory tract. In Mucosal Immunology of Acute Bacterial Pneumonia. Springer-Verlag, pp. 239.

Reyes-Jurado, F., López-Malo, A., & Palou, E. 2016: Antimicrobial activity of individual and combined essential oils against foodborne pathogenic bacteria. Journal of Food Protection, 79(2): 309–315.

Rota, M. C., Herrera, A., Martínez, R. M., Sotomayor, J. A., & Jordán, M. J. 2008. Antimicrobial activity and chemical composition of Thymus vulgaris, Thymus zygis and Thymus hyemalis essential oils. Food Control, 19(7): 681–687.

Sadiki, M., Balouiri, M., Barkai, H., Maataoui, H., Koraichi, S. I., & Elabed, S. 2014: Synergistic antibacterial effect of Myrtus communis and Thymus vulgaris essential oils fractional inhibitory concentration index. International Journal of Pharmacy and Pharmaceutical Sciences, 6(6): 121–124.

Sakkas, H., & Papadopoulou, C. 2017: Antimicrobial activity of basil, oregano, and thyme essential oils. Journal of Microbiology and Biotechnology, 27(3): 429–438.

Scandorieiro, S., de Camargo, L. C., Lancheros, C. A. C., Yamada-Ogatta, S. F., Nakamura, C. V., de Oliveira, A. G., Andrade, C. G. T. J., Duran, N., Nakazato, G., & Kobayashi, R. K. T. 2016: Synergistic and additive effect of oregano essential oil and biological silver nanoparticles against multidrug-resistant bacterial strains. Frontiers in Microbiology, 7: 1–14.

Simirgiotis, M. J., Burton, D., Parra, F., López, J., Muñoz, P., Escobar, H., & Parra, C. 2020: Antioxidant and antibacterial capacities of Origanum vulgare L. essential oil from the arid Andean region of Chile and its chemical characterization by GC-MS. Metabolites, 10(10): 1–12.

Stepanović, S., Vuković, D., Hola, V., Bonaventura, G. Di, Djukić, S., Ćircović, I., & Ruzicka, F. 2007: Quantification of biofilm in microtiter plates. Apmis, 115(8): 891–899.

Stojanović-Radić, Z., Dimitrijević, M., Genčić, M., Pejčić, M., & Radulović, N. 2020: Anticandidal activity of Inula helenium root essential oil: Synergistic potential, anti-virulence efficacy and mechanism of action. Industrial Crops and Products, 149: 112373.

Uzair, B., Niaz, N., Bano, A., Khan, B. A., Zafar, N., Iqbal, M., Tahira, R., & Fasim, F. 2017: Essential oils showing in vitro anti MRSA and synergistic activity with penicillin group of antibiotics. Pakistan Journal of Pharmaceutical Sciences, 30(5): 1997–2002.

Valizadeh, S., Mahmodi, R., Fakheri, T., Katiraie, F., & Rahmani, V. 2016: Investigating the phytochemical, antibacterial and antifungal effects of Thymus vulgaris and Cuminum cyminum essential oils. Medical Laboratory Journal, 10(1): 36–43.

Van Vuuren, S. F., Suliman, S., & Viljoen, A. M. 2009: The antimicrobial activity of four commercial essential oils in combination with conventional antimicrobials. Letters in Applied Microbiology, 48(4): 440–446.

Vázquez-Sánchez, D., Cabo, M. L., & Rodríguez-Herrera, J. J. 2014: Antimicrobial activity of essential oils against Staphylococcus aureus biofilms. Food Science and Technology International, 0(0): 1–12.

Xiao, S., Cui, P., Shi, W., & Zhang, Y. 2019: Identification of essential oils with strong activity against stationary phase Staphylococcus aureus. BioRxiv, 4: 1–10.

Zhang, D., Li, H., Gan, R., Zhu, F., Zhang, J., Wang, X., Farha, A. K., & Corke, H. 2020: Antivirulence properties and related mechanisms of spice essential oils : A comprehensive review. Comprehensive Reviews in Food Science and Food Safety, 2020: 1–39.

Figure 1. Antibiofilm activity of oregano and thyme essentail oils against the isolates of Staphylococcus aureus No. 1-6

Figure 2. Antibiofilm activity of oregano and thyme essentail oils against the isolates of Staphylococcus aureus No. 7-12

Figure 3. Time-lapse kinetics of oregano and thyme essential oils inhibitory action against Staphylococcus aureus clinical isolates (strains No. 1-6)

Figure 4. Time-lapse kinetics of oregano and thyme essential oils inhibitory action against Staphylococcus aureus clinical isolates (strains No. 7-12)


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