Anti-Bacterial Effects of Essential Oils against Uropathogenic Bacteria
Abstract
:1. Introduction
2. Results
2.1. Chemical Composition of the Essential Oils
2.2. Minimum Inhibitory and Bactericidal Concentration (MIC/MBC) Determinations
2.3. Checkerboard Assays
3. Discussion
4. Materials and Methods
4.1. Bacterial Strains and Materials
4.2. Determination of Minimal Inhibitory and Bactericidal Concentrations (MIC/MBC)
4.3. Checkerboard Assays
4.4. Statistical Analysis
Author Contributions
Funding
Conflicts of Interest
References
- Wagenlehner, F.M.E.; Pilatz, A.; Naber, K.G.; Weidner, W. Urinary tract infections. Aktuel. Urol. 2018, 45, 135–146. [Google Scholar]
- Kranz, J.; Schmidt, S.; Lebert, C.; Schneidewind, L.; Vahlensieck, W.; Sester, U.; Fünfstück, R.; Helbig, S.; Hofmann, W.; Hummers, E.; et al. Epidemiology, diagnostics, therapy, prevention and management of uncomplicated bacterial outpatient acquired urinary tract infections in adult patients: Update 2017 of the interdisciplinary AWMF S3 guideline. Urologe A 2017, 56, 746–758. [Google Scholar] [CrossRef]
- Taneja, N.; Rao, P.; Arora, J.; Dogra, A. Occurrence of ESBL and Amp-C beta-lactamases and susceptibility to newer antimicrobial agents in complicated UTI. Indian J. Med. Res. 2008, 127, 85–88. [Google Scholar]
- Dalhoff, A. Global fluoroquinolones resistance epidemiology and implications for clinical use. Interdiscip. Perspect. Infect. Dis. 2012. [Google Scholar] [CrossRef] [Green Version]
- Bakkali, F.; Averbeck, S.; Averbeck, D.; Idaomar, M. Biological effects of essential oils–A review. Food Chem. Toxicol. 2008, 46, 446–475. [Google Scholar] [CrossRef] [PubMed]
- Burt, S. Essential oils: Their antibacterial properties and potential applications in foods—A review. Int. J. Food Microbiol. 2004, 94, 223–253. [Google Scholar] [CrossRef] [PubMed]
- Mayaud, L.; Carricajo, A.; Zhiri, A.; Aubert, G. Comparison of bacteriostatic and bactericidal activity of 13 essential oils against strains with varying sensitivity to antibiotics. Lett. Appl. Microbiol. 2008, 47, 167–173. [Google Scholar] [CrossRef]
- Lee, J.H.; Kim, Y.G.; Lee, J. Carvacrol-rich oregano oil and thymol-rich thyme red oil inhibit biofilm formation and the virulence of uropathogenic Escherichia coli. J. Appl. Microbiol. 2017, 123, 1420–1428. [Google Scholar] [CrossRef]
- Zapién-Chavarría, K.A.; Plascencia-Terrazas, A.; Venegas-Ortega, M.G.; Varillas-Torres, M.; Rivera-Chavira, B.E.; Adame-Gallegos, J.R.; González-Rangel, M.O.; Nevárez-Moorillón, G.V. Susceptibility of Multidrug-Resistant and Biofilm-Forming Uropathogens to Mexican Oregano Essential Oil. Antibiotics (Basel) 2019, 8, 186. [Google Scholar] [CrossRef] [Green Version]
- Zakaria Nabti, L.; Sahli, F.; Laouar, H.; Olowo-Okere, A.; Nkuimi Wandjou, J.G.; Maggi, F. Chemical Composition and Antibacterial Activity of Essential Oils from the Algerian Endemic Origanum glandulosum Desf. against Multidrug-Resistant Uropathogenic E. coli Isolates. Antibiotics (Basel) 2020, 9, 29. [Google Scholar] [CrossRef] [Green Version]
- Wagenlehner, F.M.; Abramov-Sommariva, D.; Höller, M.; Steindl, H.; Naber, K.G. Non-Antibiotic Herbal Therapy (BNO 1045) versus Antibiotic Therapy (Fosfomycin Trometamol) for the Treatment of Acute Lower Uncomplicated Urinary Tract Infections in Women: A Double-Blind, Parallel-Group, Randomized, Multicentre, Non-Inferiority Phase III Trial. Urol. Int. 2018, 101, 327–336. [Google Scholar] [PubMed]
- 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, 1225–1228. [Google Scholar] [CrossRef]
- Scazzocchio, F.; Mondì, L.; Ammendolia, M.G.; Goldoni, P.; Comanducci, A.; Marazzato, M.; Conte, M.P.; Rinaldi, F.; Crestoni, M.E.; Fraschetti, C.; et al. Coriander (Coriandrum sativum) Essential Oil: Effect on Multidrug Resistant Uropathogenic Escherichia coli. Nat. Prod. Commun. 2017, 12, 623–626. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matsukawa, M.; Igarashi, M.; Watanabe, H.; Qin, L.; Ohnishi, M.; Terajima, J.; Iyoda, S.; Morita-Ishihara, T.; Tateda, K.; Ishii, Y.; et al. Epidemiology and genotypic characterisation of dissemination patterns of uropathogenic Escherichia coli in a community. Epidemiol. Infect. 2019, 147, e148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Longbottom, C.J.; Carson, C.F.; Hammer, K.A.; Mee, B.J.; Riley, T.V. Tolerance of Pseudomonas aeruginosa to Melaleuca alternifolia (tea tree) oil is associated with the outer membrane and energy-dependent cellular processes. J. Antimicrob. Chemother. 2004, 54, 386–392. [Google Scholar] [CrossRef]
- Ojeda-Sana, A.M.; van Baren, C.M.; Elechosa, M.A.; Juárez, M.A.; Moreno, S. New insights into antibacterial and antioxidant activities of rosemary essential oils and their main components. Food Control 2013, 31, 189–195. [Google Scholar] [CrossRef]
- Shi, C.; Song, K.; Zhang, X.; Sun, Y.; Sui, Y.; Chen, Y.; Jia, Z.; Sun, H.; Sun, Z.; Xia, X. Antimicrobial Activity and Possible Mechanism of Action of Citral against Cronobacter sakazakii. PLoS ONE 2016, 11, e0159006. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Feng, R.; Li, L.; Zhou, X.; Li, Z.; Jia, R.; Song, X.; Zou, Y.; Yin, L.; He, C.; et al. The Antibacterial Mechanism of Terpinen-4-ol Against Streptococcus agalactiae. Curr. Microbiol. 2018, 75, 1214–1220. [Google Scholar] [CrossRef]
- Liu, X.; Cai, J.; Chen, H.; Zhong, Q.; Hou, Y.; Chen, W.; Chen, W. Antibacterial activity and mechanism of linalool against Pseudomonas aeruginosa. Microb. Pathog. 2020, 141, 103980. [Google Scholar] [CrossRef]
- Nguyen, H.V.; Meile, J.C.; Lebrun, M.; Caruso, D.; Chu-Ky, S.; Sarter, S. Litsea cubeba leaf essential oil from Vietnam: Chemical diversity and its impacts on antibacterial activity. Lett. Appl. Microbiol. 2018, 66, 207–214. [Google Scholar] [CrossRef]
- Herzer, P.J.; Inouye, S.; Inouye, M.; Whittam, T.S. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J. Bacteriol. 1990, 172, 6175–6181. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Lavor, É.M.; Fernandes, A.W.C.; de Andrade Teles, R.B.; Leal, A.E.B.P.; de Oliveira Júnior, R.G.; Gama ESilva, M.; de Oliveira, A.P.; Silva, J.C.; de Moura Fontes Araújo, M.T.; Coutinho, H.D.M.; et al. Essential Oils and Their Major Compounds in the Treatment of Chronic Inflammation: A Review of Antioxidant Potential in Preclinical Studies and Molecular Mechanisms. Oxid. Med. Cell Longev. 2018, 2018, 1–23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carson, C.F.; Riley, T.V. Antimicrobial activity of the major components of the essential oil of Melaleuca alternifolia. J. Appl. Bacteriol. 1995, 78, 264–269. [Google Scholar] [CrossRef]
- Park, S.-N.; Lim, Y.K.; Freire, M.O.; Cho, E.; Jin, D.; Kook, J.-K. Antimicrobial effect of linalool and α-terpineol against periodontopathic and cariogenic bacteria. Anaerobe 2012, 18, 369–372. [Google Scholar] [CrossRef] [PubMed]
- Herman, A.; Tambor, K.; Herman, A. Linalool Affects the Antimicrobial Efficacy of Essential Oils. Curr. Microbiol. 2015, 72, 165–172. [Google Scholar] [CrossRef] [PubMed]
- Hart, P.H.; Brand, C.; Carson, C.F.; Riley, T.V.; Prager, R.H.; Finlay-Jones, J.J. Terpinen-4-ol, the main component of the essential oil of Melaleuca alternifolia (tea tree oil), suppresses inflammatory mediator production by activated human monocytes. Inflamm. Res. 2000, 49, 619–626. [Google Scholar] [CrossRef]
- Huo, M.; Cui, X.; Xue, J.; Chi, G.; Gao, R.; Deng, X.; Guan, S.; Wei, J.; Soromou, L.W.; Feng, H.; et al. Anti-inflammatory effects of linalool in RAW 264.7 macrophages and lipopolysaccharide-induced lung injury model. J. Surg. Res. 2013, 180, e47–e54. [Google Scholar] [CrossRef]
- Ninomiya, K.; Hayama, K.; Ishijima, S.A.; Maruyama, N.; Irie, H.; Kurihara, J.; Abe, S. Suppression of inflammatory reactions by terpinen-4-ol, a main constituent of tea tree oil, in a murine model of oral candidiasis and its suppressive activity to cytokine production of macrophages in vitro. Biol. Pharm. Bull. 2013, 36, 838–844. [Google Scholar] [CrossRef] [Green Version]
- Parke, D.V.; Rahman, K.H.M.Q.; Walker, R. Effect of linalool on hepatic drug-metabolizing enzymes in the rat. Biochem. Soc. Trans. 1997, 2, 615–618. [Google Scholar] [CrossRef]
- JECFA (Joint Expert Committee on Food Additives). Evaluation of Certain Food Additives and Contaminants. Forty-sixth report of the Joint FAO/WHO Expert Committee on Food Additives. WHO TRS 1997, 960, 868. [Google Scholar]
- Stickler, D.J.; Morris, N.S.; Winters, C. Simple physical model to study formation and physiology of biofilms on urethral catheters. Methods Enzymol. 1999, 310, 494–501. [Google Scholar] [PubMed]
- Eliopoulos, G.M.; Moellering, R.C., Jr. Antimicrobial combinations. In Antibiotics in Laboratory Medicine, 4th ed.; Lorian, V., Ed.; The Williams & Wilkins Co.: Baltimore, MD, USA, 1996; pp. 330–396. [Google Scholar]
Cajeput | Lemongrass | Tea Tree | Thyme | ||||
---|---|---|---|---|---|---|---|
Cambodia/wild harvesting | Nepal/organic cultivation | Australia/organic cultivation | Spain and France/organic cultivation | ||||
Steam distillation of the leaves and tops of Melaleuca leucadendron L. var cajaputi | Steam distillation of freshly cut and slightly dried grass of Cymbopogon flexuosus | Steam distillation of the leaves of Melaleuca alternifolia | Steam distillation of blooming herbs from Thymus vulgaris c.t. linalool | ||||
Batch 00284C27 and 00012A27 | Batch: 00536M26 and 00290E27 | Batch: 00040D27 | Batch: 00689F25 and 00146J26 | ||||
Component | % | Component | % | Component | % | Component | % |
α-pinene | 1.76 | camphene | 1.12–2.71 | α-thujene | 0.91 | α-pinene | 2.22–3.35 |
benzaldehyde | 0.13 | 6-methyl-5-heptene-2-one | 1.46–2.95 | α-pinene | 2.52 | camphene | 0.54–0.95 |
β-pinene | 1.27 | limonene + c-β-ocimene | 0.93–2.27 | sabinene | 0.28 | 1-octene-3-ol + sabinene | 0.82–1.12 |
myrcene | 1.23 | exo-isocitral | 0.44–0.66 | β-pinene | 0.71 | β-pinene | 0.54–0.66 |
α-terpinene | 0.23 | citronellal | 0.48–0.54 | β-myrcene | 0.84 | β-myrcene | 4.91–8.86 |
p-cymene | 0.37 | photocitral A | <0.01–0.34 | α-phellandrene | 0.44 | α-phellandrene | 0.27–0.52 |
limonene | 5.26 | isoneral | 1.13–1.80 | α-terpinene | 9.49 | α-terpinene | 2.25–4.04 |
1,8-cineol | 64.13 | isogeranial | 1.86–2.81 | p-cymene | 2.63 | p-cymene | 1.24–3.67 |
γ-terpinene | 0.74 | 1-decanal | 0.15–0.24 | limonene | 0.85 | limonene | 1.73–3.04 |
linalool | 2.69 | citronellol + nerol | 0.22–0.59 | β-phellandrene | 0.85 | β-phellandrene | 0.46–0.53 |
δ-terpineol | 0.24 | neral | 28.49–33.88 | 1,8-cineol | 2.08 | 1.8-cineol | 0.56–0.59 |
terpinen-4-ol | 0.78 | geraniol | 0.83–7.82 | γ-terpinene | 20.26 | γ-terpinene | 5.14–6.87 |
α-terpineol | 11.43 | geranial | 36.45–43.38 | ledene + bicyclogermacrene | 0.79 | c-sabinene hydrate + c-linalool oxide | 0.96–1.18 |
geraniol | 0.26 | geranyl acetate | 0.20–4.03 | linalool | 0.06 | terpinolene + t-linolool oxid | 1.19–2.06 |
eugenol | 0.04 | β-carophyllene | 0.66–1.85 | c-p-Menth-2-en-1-ol | 0.27 | linalool | 44.56–57.28 |
α-ylangene | 0.18 | isoeugenol | 0.13–0.14 | t-p-Menth-2-en-1-ol | 0.20 | hotrienol | 0.64–1.44 |
β-caryophyllene | 1.21 | γ-cadinene | 1.08–1.26 | Terpinen-4-ol | 40.39 | c-p-Menth-2-en-1-ol | 0.18–0.24 |
α-humulene | 0.80 | δ-cadinene | 0.27–0.31 | α-terpineol | 2.81 | t-p-Menth-2-en-1-ol | 0.16–0.18 |
β-selinene | 1.29 | caryophyllene oxide | 0.46–0.51 | methyleugenol | 0.05 | camphor | 0.51–0.77 |
α-selinene | 0.88 | 4-nonanone | <0.01–1.37 | t-β-caryophyllene | 0.42 | borneol | 1.10–1.61 |
guaiol | 0.66 | linalool | 1.19–1.39 | aromadendrene | 1.33 | Terpinen-4-ol | 7.57–10.51 |
β-eudesmol | 0.46 | eugenol + α-cubebene | <0.01–0.04 | allo-aromadendrene | 0.55 | α-terpineol | 1.00–1.74 |
δ-cadinene | 1.18 | c-dihydro-carvone | 0.19–0.22 | ||||
globulol | 0.29 | linalyl acetate | 0.46–2.28 | ||||
terpinolene | 3.62 | β-caryophyllene | 0.01–0.61 | ||||
6-methyl-5-heptene-2-one | <0.01–0.04 | ||||||
t-α-bergamotte | <0.01–1.71 | ||||||
m-thymol | <0.01–0.83 | ||||||
citronellol + nerol | <0.01–0.07 |
Bacterial Strain 1 | Antibiotic Resistance | Essential Oils | |||||||
---|---|---|---|---|---|---|---|---|---|
Cajeput | Lemongrass | Tea Tree | Thyme | ||||||
MIC | MBC | MIC | MBC | MIC | MBC | MIC | MBC | ||
Ec ATCC 25922 | 12.5 | 12.5 | 25 | 25 | 1.56 | 1.56 | 1.56 | 1.56 | |
Ec CHD1 | 3.13 | 3.13 | 1.56 | 3.13 | 1.56 | 1.56 | 0.78 | 1.56 | |
Ec CHD3 | 3.13 | 3.13 | 0.63 | 6.25 | 1.56 | 1.56 | 0.78 | 0.78 | |
Ec CHD22 | 3.13 | 3.13 | 25 | 25 | 1.56 | 1.56 | 1.56 | 1.56 | |
Ec CHD94 | 6.25 | 6.25 | 25 | 25 | 1.56 | 1.56 | 1.56 | 1.56 | |
Ec UTI89 | 6.25 | 6.25 | 25 | 25 | 1.56 | 1.56 | 0.78 | 0.78 | |
Ec CHD16 | blaCTX-M-15 | 6.25 | 12.5 | 12.5 | 25 | 3.13 | 6.25 | 3.13 | 3.13 |
Ec IR3 | blaCTX-M-15, blaTEM-1B | 3.13 | 6.25 | 1.56 | 1.56 | 3.13 | 3.13 | 1.56 | 3.13 |
Ec H75 | blaNDM-1 | 12.5 | 12.5 | 25 | 25 | 3.13 | 3.13 | 3.13 | 6.25 |
Ec 1949820 | fluoroquinolone | 25 | 50 | 50 | 50 | 3.13 | 0.78 | 3.13 | 3.13 |
Ec CDF2 | mcr-1 | 1.56 | 1.56 | 1.56 | 1.56 | 1.56 | 1.17 | 0.78 | 0.78 |
Kp 595 | 3.13 | 3.13 | 3.13 | 3.13 | 1.56 | 1.56 | 1.56 | 1.56 | |
Kp CHD67 | 3.13 | 3.13 | 3.13 | 6.25 | 1.56 | 1.56 | 1.56 | 1.56 | |
Kp CHD99 | 25 | 50 | 50 | 50 | 3.13 | 3.13 | 25 | 50 | |
Kp ATCC BAA1705 | blaKPC | 25 | 50 | 25 | 25 | 3.13 | 3.13 | 6.25 | 12.5 |
Kp ATCC BAA2146 | blaNDM-1 | 12.5 | 50 | 25 | 50 | 6.25 | 6.25 | 25 | 50 |
Ecl CHD57 | 25 | 50 | 25 | 25 | 1.56 | 3.13 | 1.56 | 1.56 | |
Ecl CHD60 | 3.13 | 6.25 | 6.25 | 12.5 | 0.78 | 1.56 | 0.78 | 0.78 | |
Pm CHD72 | 25 | 50 | 25 | 25 | 6.25 | 6.25 | 25 | 25 | |
Pm CHD76 | 50 | 50 | 12.5 | 25 | 6.25 | 6.25 | 25 | 25 | |
Pa ATCC 27853 | 50 | 50 | 25 | 50 | 12.5 | 50 | 25 | 50 | |
Pa CHD80 | 25 | 50 | 25 | 50 | 25 | 25 | 25 | 50 | |
Pa CHD81 | 50 | 50 | 25 | 50 | 50 | 50 | 50 | 50 | |
Ef CHD30 | 6.25 | 6.25 | 3.13 | 1.56 | 12.5 | 12.5 | 6.25 | 6.25 | |
Ef CHD31 | 12.5 | 12.5 | 1.56 | 1.56 | 12.5 | 12.5 | 6.25 | 12.5 | |
Ss Ho94 | 1.56 | 1.56 | 0.78 | 0.78 | 1.56 | 1.56 | 1.56 | 1.56 |
Essential Oil/Antibiotic | MIC | Fold Change MIC Reduction in Combination with *: | MBC | Fold Change MBC Reduction in Combination with *: | ||
---|---|---|---|---|---|---|
Tea Tree | Thyme | Tea Tree | Thyme | |||
thyme | 3.13 mg/mL | 8 # (0.531) | - | 3.13 mg/mL | 8 # (0.547) | - |
tea tree | 1.56 mg/mL | - | 8 # (0.547) | 3.13 mg/mL | - | 8 # (0.547) |
nitrofurantoin | 8 µg/mL | 2 (1) | 2 § (0.75) | 8 µg/mL | 2 § (1) | 1 (1.25) |
fosfomycin | 32 µg/mL | 2 (0.625) | 4 § (0.75) | 64 µg/mL | 4 (0.75) | 2 (0.75) |
pivmecillinam | 2 µg/mL | 4 § (0.75) | 2 § (0.75) | 8 µg/mL | 8 # (0.625) | 4 § (0.688) |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Loose, M.; Pilger, E.; Wagenlehner, F. Anti-Bacterial Effects of Essential Oils against Uropathogenic Bacteria. Antibiotics 2020, 9, 358. https://doi.org/10.3390/antibiotics9060358
Loose M, Pilger E, Wagenlehner F. Anti-Bacterial Effects of Essential Oils against Uropathogenic Bacteria. Antibiotics. 2020; 9(6):358. https://doi.org/10.3390/antibiotics9060358
Chicago/Turabian StyleLoose, Maria, Emmelie Pilger, and Florian Wagenlehner. 2020. "Anti-Bacterial Effects of Essential Oils against Uropathogenic Bacteria" Antibiotics 9, no. 6: 358. https://doi.org/10.3390/antibiotics9060358