Antimicrobial synergism and antibiofilm activities of Pelargonium graveolens, Rosemary officinalis, and Mentha piperita essential oils against extreme drug-resistant Acinetobacter baumannii clinical isolates
-
Ayse Humeyra Taskin Kafa
,
Rukiye Aslan
Abstract
Rosemary officinalis L., Pelargonium graveolens L., and Mentha piperita L., essential oils are used by complementary medicine specialists simultaneously with traditional antibiotics for treatment purposes. The chemical composition of essential oils was analyzed by the gas chromatography-mass spectrometry method. In vitro antibacterial and antibiofilm activities of the essential oils were tested against extreme drug-resistant (XDR) colistin-resistant and colistin susceptible Acinetobacter baumannii clinical strains. The synergistic activities between essential oils and colistin antibiotics were investigated by the checkerboard method. The highest antibacterial effect was detected in mint essential oil (2.5–5 μl/ml), followed by pelargonium essential oil (5–20 μl/ml) and rosemary essential oil (5–20 μl/ml). The combination of rosemary essential oil or pelargonium essential oil with colistin showed strong synergistic activity in most of the bacterial strains tested (fractional inhibitory concentration index ≤ 0.5; synergy). As a result of the combination of mint essential oil and colistin, an indifferent effect was observed in only two bacterial strains, and other strains could not be evaluated. No antagonistic effects were observed in any of the tested essential oils. As a result of the effectiveness of the combination, the minimum inhibitory concentration (MIC) values of colistin in XDR-A. baumannii clinical isolates decreased 2–32 fold. Additionally, the sub-MIC concentration of essential oils exhibited an inhibitory effect (48–90%) against the biofilm layer of tested A. baumannii strains.
Acknowledgment
We would like to thank the Cosmer Kimya company for supporting us in supplying the essential oils that we use in our study.
-
Author Contributions: A.H. Taskin Kafa participated in the design of research, conducting the experiments, analyzing the data, and drafting and commentating the manuscript. R. Aslan contributed to conducting the assays, analyzing the data, and writing the manuscript. C. Celik supervised the whole research and contributed to the continuity of assay studies. M. Hasbek contributed to the supply and preparation of bacteria, studied. All the authors have read the final manuscript and approved it.
-
Research funding: None declared.
-
Conflict of Interest Statement: No conflict of interest was declared by the authors.
References
1. Fatemi, N, Sharifmoghadam, MR, Bahreini, M, Khameneh, B, Shadifar, H. Antibacterial and synergistic effects of herbal extracts in combination with amikacin and imipenem against multidrug resistant isolates of Acinetobacter. Curr Microbiol 2020;77:1959–67. https://doi.org/10.1007/s00284-020-02105-0.Search in Google Scholar PubMed
2. Zhang, HZ, Zhang, JS, Qiao, L. The Acinetobacter baumannii group: a systemic review. World J Emerg Med 2013;4:169–74. https://doi.org/10.5847/wjem.j.issn.1920-8642.2013.03.002.Search in Google Scholar PubMed PubMed Central
3. Harding, CM, Hennon, SW, Feldman, MF. Uncovering the mechanisms of Acinetobacter baumannii virulence. Nat Rev Microbiol 2018;16:91–102. https://doi.org/10.1038/nrmicro.2017.148.Search in Google Scholar PubMed PubMed Central
4. Nazzaro, F, Fratianni, F, De Martino, L, Coppola, R, De Feo, R. Effect of essential oils on pathogenic bacteria. Pharmaceuticals 2013;6:1451–74. https://doi.org/10.3390/ph6121451.Search in Google Scholar PubMed PubMed Central
5. Dizbay, M, Altuncekic, A, Sezer, BE, et al.. Colistin and tigecycline susceptibility among multidrug-resistant Acinetobacter baumannii isolated from ventilator-associated pneumonia. Int J Antimicrob Agents 2008;32:29–32. https://doi.org/10.1016/j.ijantimicag.2008.02.016.Search in Google Scholar PubMed
6. Yau, W, Owen, RJ, Poudyal, A, et al.. Colistin heteroresistance in multi-drug-resistant Acinetobacter baumannii clinical isolates from the Western Pacific region in the SENTRY antimicrobial surveillance program. J Infect 2009;58:138–44. https://doi.org/10.1016/j.jinf.2008.11.002.Search in Google Scholar PubMed
7. Hernan, RC, Karina, B, Gabriela, G, Marcela, N, Carlos, V, Angela, F. Selection of colistin-resistant Acinetobacter baumannii isolates in post neurosurgical meningitis in an intensive care unit with high presence of hetero resistance to colistin. Diagn Microbiol Infect Dis 2009;65:188–91. https://doi.org/10.1016/j.diagmicrobio.2009.05.019.Search in Google Scholar PubMed
8. Alibi, S, Ben Selma, W, Ramos-Vivas, J, et al.. Anti-oxidant, antibacterial, anti-biofilm, and anti-quorum sensing activities of four essential oils against multidrug-resistant bacterial clinical isolates. Curr Res Transl Med 2020;68:59–66. https://doi.org/10.1016/j.retram.2020.01.001.Search in Google Scholar PubMed
9. Vasconcelos, NG, Mallmann, V, Costa, ER, Simionatto, E, Coutinho, EJ, De Lara Silva, RC, et al.. Antibacterial activity and synergism of the essential oil of Nectandra megapotamica L. flowers against OXA-23-producing Acinetobacter baumannii. J Essent Oil Res 2020;32:260–8. https://doi.org/10.1080/10412905.2020.1740802.Search in Google Scholar
10. Cacciatore, I, Di Giulio, M, Fornasari, E, Di Stefano, A, Cerasa, LS, Marinelli, L, et al.. Carvacrol codrugs: a new approach in the antimicrobial plan. PLoS One 2015;10:1–20. https://doi.org/10.1371/journal.pone.0120937.Search in Google Scholar PubMed PubMed Central
11. Chouhan, S, Sharma, K, Guleria, S. Antimicrobial activity of some essential oils-present status and future perspectives. Medicines 2017;4:58.10.3390/medicines4030058Search in Google Scholar PubMed PubMed Central
12. Magi, G, Marini, E, Facinelli, B. Antimicrobial activity of essential oils and carvacrol, and synergy of carvacrol and erythromycin, against clinical, erythromycin resistant Group A Streptococci. Front Microbiol 2016;6:165.10.3389/fmicb.2015.00165Search in Google Scholar PubMed PubMed Central
13. Magiorakos, AP, Srinivasan, A, Carey, R, Carmeli, Y, Falagas, ME, Giske, C, et al.. Multidrug-resistant, extensively drug-resistant and pan drug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268–81. https://doi.org/10.1111/j.1469-0691.2011.03570.x.Search in Google Scholar PubMed
14. Eloff, JN. A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med 1998;64:711–3. https://doi.org/10.1055/s-2006-957563.Search in Google Scholar PubMed
15. Man, A, Santacroce, L, Jacob, R, Mare, A, Man, L. Antimicrobial activity of six essential oils against a group of human pathogens: a comparative study. Pathogens 2019;8:15. https://doi.org/10.3390/pathogens8010015.Search in Google Scholar PubMed PubMed Central
16. Balouiri, M, Sadiki, M, Ibnsouda, SK. Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 2016;6:71–9. https://doi.org/10.1016/j.jpha.2015.11.005.Search in Google Scholar PubMed PubMed Central
17. Pillai, SK, Moellering, RCJ, Eliopoulus, GM. Antimicrobial combinations. In: Lorian, V, editor. Antibiotics in laboratory medicine. Philadelphia: Lippincott Williams and Wilkins; 2005:365–440 pp.Search in Google Scholar
18. Fratini, F, Mancini, S, Turchi, B, et al.. A novel interpretation of the fractional inhibitory concentration index: the case Origanum vulgare L. and Leptospermum scoparium JR et G forst essential oils against Staphylococcus aureus strains. Microbiol Res 2017;195:11–7. https://doi.org/10.1016/j.micres.2016.11.005.Search in Google Scholar PubMed
19. de Aguiar, FC, Solarte, AL, Tarradas, C, Gómez-Gascón, L, Astorga, R, Maldonado, A, et al.. Combined effect of conventional antimicrobials with essential oils and their main components against resistant Streptococcus suis strains. Lett Appl Microbiol 2019;68:562–72. https://doi.org/10.1111/lam.13151.Search in Google Scholar PubMed
20. Çelik, C, Tutar, U, Karaman, İ, Hepokur, C, Ataş, M. Evaluation of the antibiofilm and antimicrobial properties of Ziziphora tenuior L. essential oil against multidrug resistant Acinetobacter baumannii. Int J Pharmacol 2016;12:28–35.10.3923/ijp.2016.28.35Search in Google Scholar
21. Onsare, J, Arora, D. Antibiofilm potential of flavonoids extracted from Moringa oleifera seed coat against Staphylococcus aureus, Pseudomonas aeruginosa and Candida albicans. J App Microbiol 2015;118:313–25. https://doi.org/10.1111/jam.12701.Search in Google Scholar PubMed
22. Bush, K, Courvalin, P, Dantas, G, Davies, J, Eisenstein, B, Huovinen, P, et al.. Tackling antibiotic resistance. Nat Rev Microbiol 2011;9:894–6. https://doi.org/10.1038/nrmicro2693.Search in Google Scholar PubMed PubMed Central
23. Hemaiswarya, S, Kruthiventi, AK, Doble, M. Synergism between natural products and antibiotics against infectious diseases. Phytomedicine 2018;15:639–52.10.1016/j.phymed.2008.06.008Search in Google Scholar PubMed
24. Trombetta, D, Castelli, F, Sarpietro, MG, Venuti, V, Cristani, M, Daniele, C, et al.. Mechanisms of antibacterial action of three monoterpenes. Antimicrob Agents Chemother 2005:2474–8. https://doi.org/10.1128/aac.49.6.2474-2478.2005.Search in Google Scholar
25. Orchard, A, van Vuuren, S. Commercial essential oils as potential antimicrobials to treat skin diseases. Evid Based Complement Altern Med 2017:1–92. https://doi.org/10.1155/2017/4517971.Search in Google Scholar PubMed PubMed Central
26. Pintore, G, Usai, M, Bradesi, P, Juliano, C, Boatto, G, Tomi, F, et al.. Chemical composition and antimicrobial activity of Rosmarinus officinalis L. oils from Sardinia and Corsica. Flavour Fragr J 2002;1:15–9. https://doi.org/10.1002/ffj.1022.Search in Google Scholar
27. Zaouali, Y, Bouzaine, T, Boussaid, M. Essential oils composition in two Rosmarinus officinalis L. varieties and incidence for antimicrobial and antioxidant activities. Food Chem Toxicol 2010;48:3144–52. https://doi.org/10.1016/j.fct.2010.08.010.Search in Google Scholar PubMed
28. Mekonnen, A, Yitayew, B, Tesema, A, Taddese, S. In vitro antimicrobial activity of essential oil of Thymus schimperi, Matricaria chamomilla, Eucalyptus globulus, and Rosmarinus officinalis. Int J Microbiol 2016;2016:1–8. https://doi.org/10.1155/2016/9545693.Search in Google Scholar PubMed PubMed Central
29. Ghannadi, A, Bagherinejad, M, Abedi, D, Jalali, M, Absalan, B, Sadeghi, N. Antibacterial activity and composition of essential oils from Pelargonium graveolens L’Her and Vitex agnus-castus L. Iran J Microbiol 2012;4:171–6.Search in Google Scholar
30. Jiang, Y, Wu, N, Fu, YJ, Wang, W, Luo, M, Zhao, CJ, et al.. Chemical composition and antimicrobial activity of the essential oil of Rosemary. Environ Toxicol Pharmacol 2011;32:63–8. https://doi.org/10.1016/j.etap.2011.03.011.Search in Google Scholar PubMed
31. Sienkiewicz, M, Lysakowska, M, Pastuszka, M, Bienias, W, Kowalczyk, E. The potential of use Basil and Rosemary essential oils as effective antibacterial agents. Molecules 2012;18:9334–51. https://doi.org/10.1089/mdr.2011.0080.Search in Google Scholar PubMed
32. Bajalan, I, Rouzbahani, R, Pirbalouti, AG, Maggi, F. Antioxidant and antibacterial activities of the essential oils obtained from seven Iranian populations of Rosmarinus officinalis. Ind Crop Prod 2017;107:305–11. https://doi.org/10.1016/j.indcrop.2017.05.063.Search in Google Scholar
33. Probuseenivasan, S, Mayakumar, M, Ignacimuthu, S. In vitro antibacterial activity of some plant essential oils. BMC Compl Alternative Med 2006;6.10.1186/1472-6882-6-39Search in Google Scholar
34. Nieto, G, Ros, G, Castillo, J. Antioxidant and antimicrobial properties of Rosemary (Rosmarinus officinalis, L.): a review. Medicines 2018;5. https://doi.org/10.3390/medicines5030098.Search in Google Scholar
35. Cristani, M, D’Arrigo, M, Mandalari, G, Castelli, F, Sarpietro, MG, Micieli, D, et al.. Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J Agric Food Chem 2007;55:6300–8. https://doi.org/10.1021/jf070094x.Search in Google Scholar
36. Rosato, A, Carocci, A, Catalano, A, Clodoveo, ML, Franchini, C, Corbo, F, et al.. Elucidation of the synergistic action of Mentha piperita essential oil with common antimicrobials. PloS One 2018;13. https://doi.org/10.1371/journal.pone.0200902.Search in Google Scholar
37. Jarrar, N, Abu-Hijleh, A, Adwan, K. Antibacterial activity of Rosmarinus officinalis L. alone and in combination with cefuroxime against methicillin-resistant Staphylococcus aureus. Asian Pac J Trop Med 2010;3:121–3. https://doi.org/10.1016/s1995-7645(10)60049-1.Search in Google Scholar
38. Malik, T, Singh, P, Pant, S, Chauhan, N, Lohani, H. Potentiation of antimicrobial activity of ciprofloxacin by Pelargonium graveolens essential oil against selected uropathogens. Phytother Res 2011;25:1225–8. https://doi.org/10.1002/ptr.3479.Search in Google Scholar PubMed
39. Bhattamisra, SK, Kuean, CH, Chieh, LA. Antibacterial activity of geraniol in combination with standard antibiotics against Staphylococcus aureus, Escherichia coli and Helicobacter pylori. Nat Prod Commun 2018;13:791–3. https://doi.org/10.1177/1934578x1801300701.Search in Google Scholar
40. Roy, R, Tiwari, M, Donelli, G, Tiwari, V. Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence 2018;9:522–54. https://doi.org/10.1080/21505594.2017.1313372.Search in Google Scholar PubMed PubMed Central
41. Davies, D. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2003;2:114–22. https://doi.org/10.1038/nrd1008.Search in Google Scholar PubMed
42. Hengzhuang, W, Wu, H, Ciofu, O, Song, Z, Hoiby, N. Pharmacokinetics/pharmacodynamics of colistin and imipenem on mucoid and nonmucoid Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 2011;55:4469–74. https://doi.org/10.1128/aac.00126-11.Search in Google Scholar
43. Oliveira, MMM, Brugnera, DF, Cardoso, MG, Alves, E, Piccoli, RH. Disinfectant action of Cymbopogon sp. essential oils in different phases of biofilm formation by Listeria monocytogenes on stainless steel surface. Food Contr 2010;21:549–53. https://doi.org/10.1016/j.foodcont.2009.08.003.Search in Google Scholar
44. Sandasi, M, Leonard, CM, Viljoen, AM. The effect of five common essential oil components on Listeria monocytogenes biofilms. Food Contr 2008;19:1070–5. https://doi.org/10.1016/j.foodcont.2007.11.006.Search in Google Scholar
45. Chaieb, K, Kouidhi, B, Jrah, H, Mahdouani, K, Bakhrouf, A. Antibacterial activity of thymoquinone, active principle of Nigella sativa and its potency to prevent bacterial biofilm formation. BMC Compl Alternative Med 2011;11:11–29. https://doi.org/10.1186/1472-6882-11-29.Search in Google Scholar PubMed PubMed Central
46. Lagha, R, Ben Abdallah, F, Al-Sarhan, BO, Al-Sodany, Y. Antibacterial and biofilm inhibitory activity of medicinal plant essential oils against Escherichia coli isolated from UTI patients. Molecules 2019;24:1161. https://doi.org/10.3390/molecules24061161.Search in Google Scholar PubMed PubMed Central
Supplementary material
The online version of this article offers supplementary material (https://doi.org/10.1515/znc-2021-0079).
© 2021 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Research Articles
- Bioactive compounds from Matricaria chamomilla: structure identification, in vitro antiproliferative, antimigratory, antiangiogenic, and antiadenoviral activities
- Antimicrobial synergism and antibiofilm activities of Pelargonium graveolens, Rosemary officinalis, and Mentha piperita essential oils against extreme drug-resistant Acinetobacter baumannii clinical isolates
- Chemical composition, antioxidant, and antimicrobial activities of two essential oils from Algerian propolis
- Stability of proteins involved in initiation of DNA replication in UV damaged human cells
- Bioguided isolation of antiplasmodial secondary metabolites from Persea americana Mill. (Lauraceae)
- Biological activities of some Salvia species
- Secondary metabolites of downy birch buds (Betula pubescens Erch.)
- (−)-Brunneusine, a new phenolic compound with antibacterial properties in aqueous medium from the leaves of Agelanthus brunneus (Engl.) Tiegh (LORANTHACEAE)
- Novel thiazolyl-hydrazone derivatives including piperazine ring: synthesis, in vitro evaluation, and molecular docking as selective MAO-A inhibitor
Articles in the same Issue
- Frontmatter
- Research Articles
- Bioactive compounds from Matricaria chamomilla: structure identification, in vitro antiproliferative, antimigratory, antiangiogenic, and antiadenoviral activities
- Antimicrobial synergism and antibiofilm activities of Pelargonium graveolens, Rosemary officinalis, and Mentha piperita essential oils against extreme drug-resistant Acinetobacter baumannii clinical isolates
- Chemical composition, antioxidant, and antimicrobial activities of two essential oils from Algerian propolis
- Stability of proteins involved in initiation of DNA replication in UV damaged human cells
- Bioguided isolation of antiplasmodial secondary metabolites from Persea americana Mill. (Lauraceae)
- Biological activities of some Salvia species
- Secondary metabolites of downy birch buds (Betula pubescens Erch.)
- (−)-Brunneusine, a new phenolic compound with antibacterial properties in aqueous medium from the leaves of Agelanthus brunneus (Engl.) Tiegh (LORANTHACEAE)
- Novel thiazolyl-hydrazone derivatives including piperazine ring: synthesis, in vitro evaluation, and molecular docking as selective MAO-A inhibitor
