Antimicrobial and Antioxidant Effects of Emulsions and Nanoemulsions of Salvia officinalis, Pimpinella anisum, Dracocephalum moldavica, and Syzygium aromaticum Against Foodborne Bacteria

Document Type : Original Research

Authors
1 Food, Drug and Natural Products Health Research Center, Golestan University of Medical Sciences, Gorgan, Iran
2 Food, Drug and Natural Products Health Research Center, Golestan University of Medical Sciences, Gorgan, Iran.
3 Faculty of Veterinary Medicine, Science and Research Branch, Islamic Azad University, Tehran, Iran
Abstract
Due to their antimicrobial and antioxidant properties, essential oils are used as natural preservatives. The purpose of this study was to investigate the chemical composition, antioxidant properties, and antimicrobial activity of emulsion and nanoemulsion forms of Salvia officinalis, Pimpinella anisum, Dracocephalum moldavica, and Syzygium aromaticum essential oils. The Agar well-diffusion assay results obtained from the experiment suggested that nanoemulsion of Dracocephalum moldavica essential oil had the maximum antimicrobial activity against the pathogenic microorganisms drawn in the experiment. The inhibition zone diameters of the nanoemulsion of this essential oil against Shigella dysenteriae, Salmonella Typhimurium, Pseudomonas aeruginosa, Staphylococcus aureus, Listeria monocytogenes, Escherichia coli, and Bacillus cereus were 11.03, 11.82, 13.02, 13.13, 13.13, 13.62, and 14.10 mm, respectively. In contrast, the inhibition zone diameters of the emulsion form of this essential oil against S. dysenteriae, S. Typhimurium, P. aeruginosa, S. aureus, L. monocytogenes, E. coli, and B. cereus were 9.66, 10.34, 10.84, 11.84, 11.34, 11.17, and 11.24 mm, respectively. The major components of Dracocephalum moldavica essential oil included geraniol (27.24%), geranial (10.75%), alpha-copaene (8.16%), alpha-pinene (7.37%), carvacrol (7.41%), limonene (6.86%), and nerol (6.45%). The nanoemulsion form of the essential oils investigated thus possessed a significantly greater antioxidant potential compared to their emulsion form. This study also demonstrated that the nanoemulsions exhibited significantly lower IC50 values compared to the emulsions. From the results, it was seen that the nanoemulsion form of Dracocephalum moldavica essential oil had the lowest IC50 and EC50 values of 22.17 µg/ml and 4.51 µg/ml, respectively.

Keywords

Subjects


1. Abdel-Reheem, M. A., and Oraby, M. M. 2015. Anti-microbial, cytotoxicity, and necrotic ripostes of Pimpinella anisum essential oil. Ann. Agric. Sci., 60(2): 335-340.‏
2. Aćimović, M., Šovljanski, O., Šeregelj, V., Pezo, L., Zheljazkov, V. D., Ljujić, J., ... and Vujisić, L. 2022. Chemical composition, antioxidant, and antimicrobial activity of Dracocephalum moldavica L. essential oil and hydrolate. Plants, 11(7): 941.‏
3. Ali-Shtayeh, M. S., Jamous, R. M., Abu-Zaitoun, S. Y., Akkawi, R. J., Kalbouneh, S. R., Dudai, N., and Bernstein, N. 2018. Secondary treated effluent irrigation did not impact chemical composition, and enzyme inhibition activities of essential oils from Origanum syriacum var. syriacum. Ind. Crops Prod., 111: 775-786.‏
4. Alizadeh, A., Alizadeh, O., Amari, G., and Zare, M. 2013. Essential oil composition, total phenolic content, antioxidant activity and antifungal properties of Iranian Thymus daenensis subsp. daenensis Celak. as in influenced by ontogenetical variation. J. Essent. Oil Bear. Plants, 16(1): 59-70.‏
5. Baliyan, S., Mukherjee, R., Priyadarshini, A., Vibhuti, A., Gupta, A., Pandey, R. P., and Chang, C. M. 2022. Determination of antioxidants by DPPH radical scavenging activity and quantitative phytochemical analysis of Ficus religiosa. Molecules, 27(4): 1326.‏
6. Borrin, T. R., Georges, E. L., Moraes, I. C., and Pinho, S. C. 2016. Curcumin-loaded nanoemulsions produced by the emulsion inversion point (EIP) method: An evaluation of process parameters and physico-chemical stability. J. Food Eng., 169: 1-9.‏
7. Burt, S. 2004. Essential oils: their antibacterial properties and potential applications in foods—a review. Int. J. Food Microbiol., 94(3): 223-253.‏
8. Chamorro, E. R., Zambón, S. N., Morales, W. G., Sequeira, A. F., and Velasco, G. A. 2012. Study of the chemical composition of essential oils by gas chromatography. Gas Chromatography in Plant Science, Wine Technology, Toxicology and Some Specific Applications, 1: 307-324.‏
9. Couladis, M., Tzakou, O., Mimica‐Dukić, N., Jančić, R., and Stojanović, D. 2002. Essential oil of Salvia officinalis L. from Serbia and Montenegro. Flavour Fragr. J., 17(2): 119-126.‏
10. Delamare, A. P. L., Moschen-Pistorello, I. T., Artico, L., Atti-Serafini, L., and Echeverrigaray, S. 2007. Antibacterial activity of the essential oils of Salvia officinalis L. and Salvia triloba L. cultivated in South Brazil. Food Chem., 100(2): 603-608.‏
11. Eghbal, H., Mohammadi, A., Mohammad Nejad Khiavi, N., Ahmadi Sabegh, M., and Jahani, N. 2021. Comparison of the antibacterial properties of essential oils of Malva sylvestris and Salvia officinalis on common bacteria of oral infection with chlorhexidine mouthwash. J. Mashhad Dent. Sch., 45(3): 217-229.‏
12. El-Baky, H. A., and El-Baroty, G. S. 2008. Chemical and biological evaluation of the essential oil of Egyptian Moldavian balm.‏ Int. J. Essent. Oil Ther., 2: 78-81.
13. Erkan, N., Ayranci, G., and Ayranci, E. 2008. Antioxidant activities of rosemary (Rosmarinus Officinalis L.) extract, blackseed (Nigella sativa L.) essential oil, carnosic acid, rosmarinic acid and sesamol. Food Chem., 110(1): 76-82.‏
14. Fichi, G., Flamini, G., Giovanelli, F., Otranto, D., and Perrucci, S. 2007. Efficacy of an essential oil of Eugenia caryophyllata against Psoroptes cuniculi. Expe. Parasitol., 115(2): 168-172.‏
15. Ghosh, V., Mukherjee, A., and Chandrasekaran, N. 2013. Formulation and characterization of plant essential oil based nanoemulsion: evaluation of its larvicidal activity against Aedes aegypti. Asian J. Chem., 25 (Supplementary Issue): S321.‏
16. Grausgruber-Gröger, S., Schmiderer, C., Steinborn, R., and Novak, J. 2012. Seasonal influence on gene expression of monoterpene synthases in Salvia officinalis (Lamiaceae). J. Plant Physiol., 169(4): 353-359.‏
17. Hakkak, M., Hozni S., Morovati, H. and Akhlaghi, T. 2018. Research Diagnosis in Postgraduate Students of Guilan University of Medical Sciences. Res. Med. Educ., 10(2): 46-57
18. Hendawy, S. F., El Gendy, A. G., Omer, E. A., Pistelli, L., and Pistelli, L. 2018. Growth, yield and chemical composition of essential oil of Mentha piperita var. multimentha grown under different agro-ecological locations in Egypt. J. Essent. Oil Bear. Plants, 21(1): 23-39.‏
19. Holm, Y., Hiltunen, R., and Nykanen, I. 1988. Capillary gas chromatographic‐mass spectrometric determination of the flavour composition of dragonhead (Dracocephalum moldavica L.). Flavour Fragr. J., 3(3): 109-112.‏
20. Kakasy, A. Z., Lemberkovics, E., Simandi, B., Lelik, L., Hethelyi, E., Antal, I., and Szöke, É. 2006. Comparative study of traditional essential oil and supercritical fluid extracts of Moldavian dragonhead (Dracocephalum moldavica L.). Flavour Fragr. J., 21(4), 598-603.‏
21. Kelen, M., and Tepe, B. 2008. Chemical composition, antioxidant and antimicrobial properties of the essential oils of three Salvia species from Turkish flora. Bioresour. Technol., 99(10): 4096-4104.‏
22. Kennouche, A., Benkaci-Ali, F., Scholl, G., and Eppe, G. 2015. Chemical composition and antimicrobial activity of the essential oil of Eugenia caryophyllata cloves extracted by conventional and microwave techniques. J. Biol. Active Prod. Nature, 5(1): 1-11.‏
23. Kumar, N., and Goel, N. 2019. Phenolic acids: Natural versatile molecules with promising therapeutic applications. Biotech. Rep., 24: e00370.‏
24. Lira, M. H. P. D., Andrade Júnior, F. P. D., Moraes, G. F. Q., Macena, G. D. S., Pereira, F. D. O., and Lima, I. O. 2020. Antimicrobial activity of geraniol: An integrative review. J. Essent. Oil Res., 32(3): 187-197.
25. Liu, Q., and Yao, H. 2007. Antioxidant activities of barley seeds extracts. Food Chem., 102(3): 732-737.‏
26. Maham, M., Akbari, H., and Delazar, A. 2013. Chemical composition and antinociceptive effect of the essential oil of Dracocephalum moldavica L. Pharm. Sci., 18(4):187-192.‏
27. McClements, D. J. 2012. Nanoemulsions versus microemulsions: terminology, differences, and similarities. Soft Matter, 8(6): 1719-1729.‏
28. McClements, D. J., and Rao, J. 2011. Food-grade nanoemulsions: formulation, fabrication, properties, performance, biological fate, and potential toxicity. Crit. Rev. Food Sci. Nutr., 51(4): 285-330.‏
29. Mirtaghi, S. M., Nejad, P. T., Masoumeh Mazandarani, M., Livani, F., and Bagheri, H. 2016. Evaluation of Antibacterial Activity of Urtica dioica L. Leaf Ethanolic Extract Using Agar Well Diffusion and Disc Diffusion Methods. Med. Lab. J., 10(5): 15-21.
30. Moghimi, R., Ghaderi, L., Rafati, H., Aliahmadi, A., and McClements, D. J. 2016. Superior antibacterial activity of nanoemulsion of Thymus daenensis essential oil against E. coli. Food Chem., 194: 410-415.
31. Myint, S., Daud, W. R. W., Mohamad, A. B., and Kadhum, A. A. H. 1996. Gas chromatographic analysis of eugenol in alcohol clove extract of cloves. J. Chromatogr. B., 679: 193-195.‏
32. Nassar, M. I., Gaara, A. H., El-Ghorab, A. H., Farrag, A., Shen, H., Huq, E., and Mabry, T. J. 2007. Chemical constituents of clove (Syzygium aromaticum, Fam. Myrtaceae) and their antioxidant activity. Rev. Latinoam. Quím., 35(3): 47.‏
33. Nazemisalman, B., Taheri, S. S., Heidari, F., Yazdinezhad, A., Haghi, F., Shabouei Jam, M., and Basir Shabestari, S. 2024. Comparison of dracocephalum Moldavica essential oil with chlorhexidine on cariogenic bacteria. J. Dent., 25(3): 223-228.‏
34. Nazzaro, F., Fratianni, F., De Martino, L., Coppola, R., and De Feo, V. 2013. Effect of essential oils on pathogenic bacteria. Pharmaceuticals, 6(12): 1451-1474.‏
35. Orav, A., Raal, A., and Arak, E. 2008. Essential oil composition of Pimpinella anisum L. fruits from various European countries. Nat. Prod. Res., 22(3): 227-232.‏
36. Oyaizu, M. (1986). Antioxidative activities of browning reaction prepared from glucosamine. Jap. J. Nutr. Diet., 44, 307-315.
37. Perugini Biasi-Garbin, R., Saori Otaguiri, E., Morey, A. T., Fernandes da Silva, M., Belotto Morguette, A. E., Armando Contreras Lancheros, C., ... and Yamada-Ogatta, S. F. 2015. Effect of eugenol against Streptococcus agalactiae and synergistic interaction with biologically produced silver nanoparticles. Evid. Based Complement. Alternat. Med., 2015(1): 861497.‏
38. Purkait, S., Bhattacharya, A., Bag, A., and Chattopadhyay, R.R. 2018. Evaluation of antibacterial and antioxidant activities of essential oils of fve spices. J. Food Qual. Hazards Control, 5(2): 61–71.
39. Rao, J., and McClements, D. J. 2011. Food-grade microemulsions, nanoemulsions and emulsions: Fabrication from sucrose monopalmitate & lemon oil. Food Hydrocoll., 25(6): 1413-1423.‏
40. Ruiz-Navajas, Y., Viuda-Martos, M., Sendra, E., Perez-Alvarez, J. A., and Fernández-López, J. 2012. Chemical characterization and antibacterial activity of Thymus moroderi and Thymus piperella essential oils, two Thymus endemic species from southeast of Spain. Food Control, 27(2): 294-299.‏
41. Shahabi, N., Tajik, H., Moradi, M., Forough, M., and Ezati, P. 2017. Physical, antimicrobial and antibiofilm properties of Zataria multiflora Boiss essential oil nanoemulsion. Int. J. Food Sci. Technol., 52(7): 1645-1652. ‏
42. Shahbazi, Y., Shavisi, N., Modarresi, M., and Karami, N. 2016. Chemical composition, antibacterial and antioxidant activities of essential oils from the aerial parts of Ferulago angulata (Schlecht.) Boiss and Ferulago bernardii Tomk. & M. Pimen from different parts of Iran. J. Essent. Oil Bear. Plants, 19(7): 1627-1638.‏
43. Shavisi, N., Khanjari, A., Basti, A. A., Misaghi, A., and Shahbazi, Y. 2017. Effect of PLA films containing propolis ethanolic extract, cellulose nanoparticle and Ziziphora clinopodioides essential oil on chemical, microbial and sensory properties of minced beef. Meat Sci., 124: 95-104.‏
44. Singh, G., Kapoor, I. P. S., de Heluani, C. S., and Catalan, C. A. N. 2008. Chemical composition and antioxidant potential of essential oil and oleoresins from anise seeds (Pimpinella anisum L.).‏ Int. J. Essent. Oil Ther., 2: 122-130
45. Skandamis, P., Koutsoumanis, K., Fasseas, K., and Nychas, G. J. E. 2001. Inhibition of oregano essential oil and EDTA on Escherichia coli O157: H7.‏ Ital. J. Food Sci., 13(1): 65-75.
46. Sonboli, A., Mojarrad, M., Gholipour, A., Ebrahimi, S. N., and Arman, M. 2008. Biological activity and composition of the essential oil of Dracocephalum moldavica L. grown in Iran. Nat. Prod. Commun., 3(9): 1934578X0800300930.‏
47. Topuz, O. K., Özvural, E. B., Zhao, Q., Huang, Q., Chikindas, M., and Gölükçü, M. 2016. Physical and antimicrobial properties of anise oil loaded nanoemulsions on the survival of foodborne pathogens. Food Chem., 203: 117-123.
48. Turgis, M., Vu, K. D., Dupont, C., and Lacroix, M. 2012. Combined antimicrobial effect of essential oils and bacteriocins against foodborne pathogens and food spoilage bacteria. Food Res. Int., 48(2), 696-702.‏
49. Ullah, H., Mahmood, A., and Honermeier, B. 2014. Essential oil and composition of anise (Pimpinella anisum L.) with varying seed rates and row spacing. Pak. J. Bot., 46(5): 1859-1864.‏
50. Wójtowicz, A., Oniszczuk, A., Oniszczuk, T., Kocira, S., Wojtunik, K., Mitrus, M., ... and Skalicka-Woźniak, K. 2017. Application of Moldavian dragonhead (Dracocephalum moldavica L.) leaves addition as a functional component of nutritionally valuable corn snacks. J. Food Sci. Technol., 54: 3218-3229.‏
51. Yousefzadeh, S., Modarres-Sanavy, S. A. M., Sefidkon, F., Asgarzadeh, A., Ghalavand, A., and Sadat-Asilan, K. 2013. Effects of Azocompost and urea on the herbage yield and contents and compositions of essential oils from two genotypes of dragonhead (Dracocephalum moldavica L.) in two regions of Iran. Food Chem., 138(2-3):1407-1413.‏

Articles in Press, Accepted Manuscript
Available Online from 01 January 2024