Evaluation of Antibacterial Activity of Commercial Lemon, Geranium, and Thistle Oils Against Pseudomonas Species

Abstract

Increasing antibiotic resistance is increasingly affecting human and animal health. Pseudomonas spp. are opportunistic pathogens resistant to multiple antibiotics. Pseudomonas spp. can be found in various environmental sources, including surface water, wastewater, food, and soil, and can cause hospital-associated infections. Therefore, due to the increasing resistance to antibiotics, plants and their extracts are being investigated as alternative natural sources of antibiotics. Thus, in this study, the antibacterial activities of commercially available thistle (Silybum marianum) fixed oil, lemon (Citrus limon), and geranium (Pelargonium graveolens) essential oils against Pseudomonas aeruginosa, Pseudomonas putida, and Pseudomonas monteilii isolated from used makeup sponges, as well as Pseudomonas aeruginosa ATCC 27853 and ATCC 10145, were evaluated in vitro using agar well diffusion and microdilution methods. It was determined that thistle fixed oil, lemon, and geranium essential oils did not give an inhibition zone against the tested Pseudomonas species, and their MIC values were greater than 80 μg/mL.

Keywords

• Citrus limon
• Pelargonium graveolens
• Silybum marianum
• Pseudomonas species
• Antibacterial activity

Ticari Limon, Sardunya (Itır) ve Deve Dikeni Yağlarının Pseudomonas Türlerine Karşı Antibakteriyel Aktivitesinin Değerlendirilmesi

Abstract

Artan antibiyotik direnci insan ve hayvan sağlığını her geçen gün etkilemektedir. Pseudomonas türleri ise birden çok antibiyotiğe karşı dirençli fırsatçı bir patojendir. Pseudomonas türleri yüzey suyu, atık su, gıda ve toprak gibi çevresel kaynaklardan da bulunabilmekte ve hastane ilişkili enfeksiyonlara neden olmaktadır. Bu nedenle artan antibiyotik direnci sebebiyle de antibiyotiklere alternatif doğal kaynaklar olan bitkiler ve onların ekstraktları araştırılmaktadır. Bu nedenle bu çalışmada kullanılmış makyaj süngerlerinden izole edilmiş Pseudomonas aeruginosa, Pseudomonas putida, Pseudomonas monteilii izolatları ile Pseudomonas aeruginosa ATCC 27853 ve ATCC 10145’e karşı ticari olarak satılan deve dikeni (Silybum marianum) sabit yağı, limon (Citrus limon) ve sardunya (Pelargonium graveolens) uçucu yağlarının antibakteriyel aktivitesi karşı agar kuyu difüzyon ve mikrodilüsyon yöntemiyle in vitro olarak değerlendirilmiştir. Test edilen Pseudomonas türlerine deve dikeni sabit yağı, limon ve sardunya uçucu yağlarının inhibisyon zonu oluşturmadığı ve MİK değerlerinin >80 μL/mL olduğu tespit edilmiştir.

Keywords

• Citrus limon
• Pelargonium graveolens
• Silybum marianum
• Pseudomonas türleri
• Antibakteriyel aktivite

References

1. Abenavoli, L., Izzo, A. A., Milić, N., Cicala, C., Santini, A., Capasso, R., 2018. Milk thistle (Silybum marianum): A concise overview on its chemistry, pharmacological, and nutraceutical uses in liver diseases. Phytotherapy research, 32 (11): 2202–2213. https://doi.org/10.1002/ptr.6171
2. Amorim, J. L., Simas, D. L. R., Pinheiro, M. M. G., Moreno, D. S. A., Alviano, C. S., da Silva, A. J. R., Dias Fernandes, P., 2016. Anti-inflammatory properties and chemical characterization of the essential oils of four citrus species. PloS one, 11 (4): e0153643. https://doi.org/10.1371/journal.pone.0153643
3. Angane, M., Swift, S., Huang, K., Butts, C. A., Quek, S. Y., 2022. Essential oils and their major components: An updated review on antimicrobial activities, mechanism of action and their potential application in the food industry. Foods, 11 (3): 464. https://doi.org/10.3390/foods11030464
4. Asker, M., El-Gengaihi, S. E., Hassan, E. M., Mohammed, M. A., Abdelhamid, S. A., 2020. Phytochemical constituents and antibacterial activity of Citrus lemon leaves. Bulletin of the National Research Centre, 44: 1–7. https://doi.org/10.1186/s42269-020-00446-1
5. Bajpai, V. K., Baek, K. H., Kang, S. C., 2012. Control of Salmonella in foods by using essential oils: A review. Food Research International, 45 (2): 722–734. https://doi.org/10.1016/j.foodres.2011.04.052
6. Bajwa, A., Tariq, S., Yuchi, A., Hafeez, R., Arshad, A., Zaman, M., Aqeel, T., Mushtaq, M. N., 2016. Evaluation of anti-bacterial activity of Silybum marianum against pathogenic and resistant bacteria. European journal of medicinal plants, 13 (4): 1–7. https://doi.org/10.9734/EJMP/2016/24732.
7. Barut Gök, S., Pehlivan, EC, Aydın, M., Erdoğdu, Y., 2020. Silybum marianum L. Tohumlarının Yağ Asitleri Bileşimi ve Tohum Yağı ve Siliymarin Ekstresinin Antimikrobiyal Aktivitesi. Gıda, 46 (1): 110–118. https://doi.org/10.15237/gida.GD20106
8. Ben Hsouna, A., Ben Halima, N., Smaoui, S., Hamdi, N., 2017. Citrus lemon essential oil: Chemical composition, antioxidant and antimicrobial activities with its preservative effect against Listeria monocytogenes inoculated in minced beef meat. Lipids in health and disease, 16: 1–11. https://doi.org/10.1186/s12944-017-0487-5

9. Bigos, M., Wasiela, M., Kalemba, D., Sienkiewicz, M., 2012. Antimicrobial activity of geranium oil against clinical strains of Staphylococcus aureus. Molecules, 17 (9): 10276–10291. https://doi.org/10.3390/molecules170910276
10. Bouzenna, H., Dhibi, S., Samout, N., Rjeibi, I., Talarmin, H., Elfeki, A., Hfaiedh, N., 2016. The protective effect of Citrus limon essential oil on hepatotoxicity and nephrotoxicity induced by aspirin in rats. Biomedicine & pharmacotherapy, 83: 1327–1334. https://doi.org/10.1016/j.biopha.2016.08.037
11. Breidenstein, E. B., de la Fuente-Núñez, C., Hancock, R. E. (2011). Pseudomonas aeruginosa: all roads lead to resistance. Trends in microbiology, 19(8): 419–426. https://doi.org/10.1016/j.tim.2011.04.005
12. Burt, S. 2004. Essential oils: Their antibacterial properties and potential applications in foods—A review. International Journal of Food Microbiology, 94 (3): 223–253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
13. Chouhan, S., Sharma, K., Guleria, S., 2017. Antimicrobial activity of some essential oils—present status and future perspectives. Medicines, 4 (3): 58. https://doi.org/10.3390/medicines4030058
14. De Oliveira, D. M., Forde, B. M., Kidd, T. J., Harris, P. N., Schembri, M. A., Beatson, S. A., Paterson, D. L., Walker, M. J., 2020 . Antimicrobial resistance in ESKAPE pathogens. Clinical microbiology reviews, 33 (3): 1110–1128. https://doi.org/10.1128/cmr.00181-19
15. de Rapper, S., Kamatou, G., Viljoen, A., van Vuuren, S., 2013. The in vitro antimicrobial activity of Lavandula angustifolia essential oil in combination with other aroma‐therapeutic oils. Evidence‐Based Complementary and Alternative Medicine, 2013 (1): 852049. https://doi.org/10.1155/2013/852049
16. Denissen, J., Reyneke, B., Waso-Reyneke, M., Havenga, B., Barnard, T., Khan, S., Khan, W., 2022. Prevalence of ESKAPE pathogens in the environment: Antibiotic resistance status, community-acquired infection and risk to human health. International journal of hygiene and environmental health, 244: 114006. https://doi.org/10.1016/j.ijheh.2022.114006
17. Evren, E., Yurtcu, E., 2015. In vitro effects on biofilm viability and antibacterial and antiadherent activities of silymarin. Folia microbiologica, 60 (4): 351–356, https://doi.org/10.1007/s12223-015-0399-6
18. Fisher, K., Phillips, C., 2008. Potential antimicrobial uses of essential oils in food: is citrus the answer?. Trends in Food Science & Technology, 19 (3): 156–164. https://doi.org/10.1016/j.tifs.2007.11.006
19. Ghannadi, A., Bagherinejad, M. R., Abedi, D., Jalali, M., Absalan, B., Sadeghi, N., 2012. Antibacterial activity and composition of essential oils from Pelargonium graveolens L'Her and Vitex agnus-castus L. Iranian journal of microbiology, 4 (4): 171–176.https://ijm.tums.ac.ir/index.php/ijm/article/view/681
20. Ghoorchibeigi, M. O. N. A., Larijani, K., Azar, P. A., Zare, K., Mehregan, I., 2017. Chemical composition and radical scavenging activity of Citrus limon peel essential oil. Oriental Journal of Chemistry, 33: 458–461. https://doi.org/10.13005/ojc/330153
21. Hadj Larbi, N., Moghrani, H., Nasrallah, N., Benelmouffok, A., Kellou, D., 2023. Influence of harvest season on the chemical composition and antifungal activity of Citrus limon essential oil. Rendiconti Lincei. Scienze Fisiche e Naturali, 34 (1): 295–303. https://doi.org/10.1007/s12210-023-01132-w
22. Hancock, R. E., Speert, D. P., 2000. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug resistance updates, 3 (4): 247–255. https://doi.org/10.1054/drup.2000.0152
23. Hsouna, A. B., Hamdi, N., 2012. Phytochemical composition and antimicrobial activities of the essential oils and organic extracts from Pelargonium graveolens growing in Tunisia. Lipids in health and disease, 11: 1–7. https://doi.org/10.1186/1476-511X-11-167
24. Janeczko, M., Kochanowicz, E., 2019. Silymarin, a Popular Dietary Supplement Shows Anti-Candida Activity. Antibiotics, 8 (4): 206. https://doi.org/10.3390/antibiotics8040206
25. Kačániová, M., Čmiková, N., Vukovic, N. L., Verešová, A., Bianchi, A., Garzoli, S., Saad, R. B., Ben Hsouna, A., Ban, Z., Vukic, M. D., 2024. Citrus limon essential oil: chemical composition and Selected biological properties focusing on the antimicrobial (in vitro, in situ), Antibiofilm, Insecticidal activity and preservative effect against Salmonella enterica inoculated in carrot. Plants, 13 (4): 524. https://doi.org/10.3390/plants13040524
26. Klockgether, J., Tümmler, B., 2017. Recent advances in understanding Pseudomonas aeruginosa as a pathogen. F1000Research, 6: 1261. https://doi.org/10.12688/f1000research.10506.1
27. Kolodziej, H., Kayser, O., Radtke, O. A., Kiderlen, A. F., Koch, E., 2003. Pharmacological profile of extracts of Pelargonium sidoides and their constituents. Phytomedicine, 10: 18–24. https://doi.org/10.1078/1433-187X-00307
28. Latté, K. P., Kolodziej, H., 2004. Antioxidant properties of phenolic compounds from Pelargonium reniforme. Journal of Agricultural and Food Chemistry, 52 (15): 4899–4902. https://doi.org/10.1021/jf0495688
29. Lee, W., Lee, D. G., 2018. Potential role of potassium and chloride channels in regulation of silymarin-induced apoptosis in Candida albicans. IUBMB Life, 70 (3): 197– 206. https://doi.org/10.1002/iub.1716
30. Miller, W. R., Arias, C.A. 2024. ESKAPE pathogens: antimicrobial resistance, epidemiology, clinical impact and therapeutics. Nature Reviews Microbiology, 22 (10): 598–616. https://doi.org/10.1038/s41579-024-01054-w
31. Nikolić, M. M., Jovanović, K. K., Marković, T. L., Marković, D. L., Gligorijević, N. N., Radulović, S. S., Kostić, M., Glamočlija, J. M., Soković, M. D., 2017. Antimicrobial synergism and cytotoxic properties of Citrus limon L., Piper nigrum L. and Melaleuca alternifolia (Maiden and Betche) Cheel essential oils. Journal of Pharmacy and Pharmacology, 69 (11): 1606–1614. https://doi.org/10.1111/jphp.12792
32. Özcan Ateş G, Bican Süerdem T., 2024. Antibacterial and Antifungal Activity of Abies nordmanniana subsp. equi-trojani (Aschers. & Sint. ex Boiss) Extracts. Sinop Üniversitesi Fen Bilimleri Dergisi, 9 (1): 184–193. https://doi.org/10.33484/sinopfbd.1404628
33. Pachori, P., Gothalwal, R., Gandhi, P., 2019. Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes & diseases, 6(2): 109–119. https://doi.org/10.1016/j.gendis.2019.04.001
34. Pasquariello, M., Martinelli, T., Paris, R., Moschella, A., Colombo, R., Di Bello, A., Frigerio, J., Kheloufi, A., Mirzaabolghasemi, M. A., Puglisi, D., Esposito, S., Scalercio, S., Virzì, N., De Vita, P., Pecchioni, N., Bassolino, L., 2025. Exploring the chemotypic variability of Silybum marianum and Silybum eburneum by biochemical and genetic characterization. Frontiers in Plant Science, 16: 1584104. https://doi.org/10.3389/fpls.2025.1584104
35. Poole, K., 2011. Pseudomonas aeruginosa: resistance to the max. Frontiers in microbiology, 2: 65. https://doi.org/10.3389/fmicb.2011.00065
36. Reverchon, E., De Marco, I., 2006. Supercritical fluid extraction and fractionation of natural matter. The Journal of Supercritical Fluids, 38 (2): 146–166. https://doi.org/10.1016/j.supflu.2006.03.020
37. Rozza, A. L., de Mello Moraes, T., Kushima, H., Tanimoto, A., Marques, M. O. M., Bauab, T. M., Hiruma-Lima, C. A., Pellizzon, C. H., 2011. Gastroprotective mechanisms of Citrus lemon (Rutaceae) essential oil and its majority compounds limonene and β-pinene: Involvement of heat-shock protein-70, vasoactive intestinal peptide, glutathione, sulfhydryl compounds, nitric oxide and prostaglandin E2. Chemico-biological interactions, 189 (1-2): 82–89. https://doi.org/10.1016/j.cbi.2010.09.031
38. Shah, S. M. M., Khan, F. A., Shah, S. M. H., Chishti, K. A., Pirzada, S. M. S. S., Khan, M. A., Farid, A., 2011. Evaluation of phytochemicals and antimicrobial activity of white and blue capitulum and whole plant of Silybum marianum. World Applied Sciences Journal, 12 (8): 1139–1144. http://www.idosi.org/wasj/wasj12(8)/2.pdf
39. Tacconelli, E., Sifakis, F., Harbarth, S., Schrijver, R., van Mourik, M., Voss, A., Sharland, M., Rajendran, N. B., Rodríguez-Baño, J., 2018. Surveillance for control of antimicrobial resistance. The Lancet Infectious Diseases, 18 (3): e99–e106. https://doi.org/10.1016/S1473-3099(17)30485-1
40. Tang, K. W. K., Millar, B. C., Moore, J. E., 2023. Antimicrobial resistance (AMR). British journal of biomedical science, 80: 11387. https://doi.org/10.3389/bjbs.2023.11387
41. Tuon, F. F., Dantas, L. R., Suss, P. H., & Tasca Ribeiro, V. S., 2022. Pathogenesis of the Pseudomonas aeruginosa Biofilm: A Review. Pathogens, 11(3): 300. https://doi.org/10.3390/pathogens11030300
42. Viana, M. D. M., Cardoso, R. M., Silva, N. K. G. T., Falcão, M. A. P., Vieira, A. C. S., Alexandre-Moreira, M. S., Campesatto, E. A., 2016. Anxiolytic-like effect of Citrus limon (L.) Burm f. essential oil inhalation on mice. Revista Brasileira de Plantas Medicinais, 18: 96–104. https://doi.org/10.1590/1983-084X/15_047
43. Wang, X., Zhang, Z., Wu, S. C., 2020. Health benefits of Silybum marianum: Phytochemistry, pharmacology, and applications. Journal of agricultural and food chemistry, 68 (42): 11644–11664. https://doi.org/10.1021/acs.jafc.0c04791
44. Yun, D. G., Lee, D. G., 2016. Silibinin triggers yeast apoptosis related to mitochondrial Ca(2+) influx in Candida albicans. The international journal of biochemistry & cell biology, 80: 1– 9. https://doi.org/10.1016/j.biocel.2016.09.008
45. Yun, D. G., Lee, D. G., 2017a. Assessment of silibinin as a potential antifungal agent and investigation of its mechanism of action. IUBMB Life, 69 (8): 631– 637. https://doi.org/10.1002/iub.1647
46. Yun, D. G., Lee, D. G., 2017b. Silymarin exerts antifungal effects via membrane-targeted mode of action by increasing permeability and inducing oxidative stress. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1859(3): 467– 474. https://doi.org/10.1016/j.bbamem.2017.01.009