In Vitro Inhibitory Effect of Four Essential Oils against Fluoroquinolone- Resistant Enterobacteriaceae Responsible for Community-Acquired Urinary Tract Infections

Main Article Content

Fatma Mahdi
Mohammed Salih Barka
Mourad Bendahou
Saida Ouslimani
Mohammed Yacine Benziane
Alain Muselli

Abstract

The emergence of antibiotic resistance genes has highlighted the need to discover new drugs for the treatment of infections caused by multidrug-resistant bacteria. The study aims to investigate the antibacterial and anti-adhesive effect of four essential oils (EOs) from aromatic medicinal plants: Ammoides verticillata, Origanum glandulosum, Thymus fontanesii, and Thymus capitatus, against fluoroquinolones-resistant uropathogenic Enterobacteriaceae. The chemical composition of the oils was determined by gas chromatography-mass spectrometry GC/MS, the antibacterial activity was assessed using disc diffusion and micro-dilution methods, while the adhesion assay was carried out using light microscopy. The essential oils of Thymus fontanesii and Thymus capitatus were carvacrol chemotype, whereas Ammoides verticillata and Origanum glandulosum EOs were thymol chemotype. Sixteen Enterobacteriaceae with different fluoroquinolones-resistance profiles were isolated, belonging to Escherichia coli, Klebsiella pneumoniae and Proteus mirabilis species. The inhibition zone diameters ranged from 17.67 ± 0.58 to 31 ± 0.00 (mm), Thymus capitatus EO appears to be the most effective, with the minimum inhibitory concentrations ranging from 0.5 mg/mL to 7.5 mg/mL. The lowest MIC (0.5 mg/mL) was observed for Thymus capitatus EO against Escherichia coli resistant strains. The adhesion assay showed a good adhesion reduction of the test Escherichia coli for all EOs, varying from 79% to 90%. These findings indicate that the studied essential oils can be used as a promising drug in the prevention and treatment of infections caused by resistant Enterobacteriaceae, however, exploring their therapeutic use requires thorough investigations that involves rigorous clinical studies to ensure their safety and efficacy.

Downloads

Download data is not yet available.

Article Details

How to Cite
Mahdi, F., Barka, M. S., Bendahou, M., Ouslimani, S., Benziane, M. Y., & Muselli, A. (2024). In Vitro Inhibitory Effect of Four Essential Oils against Fluoroquinolone- Resistant Enterobacteriaceae Responsible for Community-Acquired Urinary Tract Infections. Tropical Journal of Natural Product Research (TJNPR), 8(8), 8233-8243. https://doi.org/10.26538/tjnpr/v8i8.46
Section
Articles

References

Donkor ES, Horlortu PZ, Dayie NT, Obeng-Nkrumah N, Labi AK. Community acquired urinary tract infections among adults in Accra, Ghana. Infect. Drug Resist. 2019; 12(1): 2059-2067.

Aderibigbe SA, Alabi OS, Yekini QA. Evaluation of Nauclea diderrichii (de wild.) Merrill leaf extracts and fractions against some clinical bacterial isolates from urinary tract infections. Trop. J. Nat. Prod. Res. 2019; 3(7): 231–234.

Armand-Lefèvre L. Resistance in the city, myth or reality? The threat of ESBL-producing Enterobacteria. J. Antiinfect. 2017; 19 (1): 1-6.

Skalet AH, Cevallos V, Ayele B, Gebre T, Zhou Z, Jorgensen JH, Zerihun M, Habte, Assefa Y, Emerson PM, Gaynor BD, Porco TC, Lietman TM, Keenan JD. Antibiotic selection pressure and macrolide resistance in nasopharyngeal Streptococcus pneumoniae: a cluster-randomized clinical trial. PLoS med. 2010; 7(12): 377.

Al Zuhairi JJMJ, Kashi FJ, Rahimi-Moghaddam A, Yazdani M. Antioxidant, cytotoxic and antibacterial activity of Rosmarinus officinalis L. essential oil against bacteria isolated from urinary tract infection. Eur. J. Integr. Med. 2020; 38: 101192.

Mihankhah A, Khoshbakht R, Raeisi M, Raeisi V. Prevalence and antibiotic resistance pattern of bacteria isolated from urinary tract infections in Northern Iran. J. Res. Med. Sci. 2017; 22.

Dalhoff A. Global fluoroquinolone resistance epidemiology and implictions for clinical use. Interdiscip. Perspect. Infect. Dis. 2012; 2012(1): 976273

Kotb DN, Mahdy WK, Mahmoud MS, Khairy RM. Impact of co-existence of PMQR genes and QRDR mutations on fluoroquinolones resistance in Enterobacteriaceae strains isolated from community and hospital acquired UTIs. BMC Infect. Dis. 2019; 19: 1-8.

Ghafari O, Sharifi A, Ahmadi A, Nayeri Fasaei B. Antibacterial and anti‐PmrA activity of plant essential oils against fluoroquinolone‐resistant Streptococcus pneumoniae clinical isolates. Lett. Appl. Microbiol. 2018; 67(6): 564-569.

Soulaimani B, El Hidar N, El Fakir SB, Mezrioui N, Hassani L, Abbad A. Combined antibacterial activity of essential oils extracted from Lavandula maroccana (Murb.), Thymus pallidus Batt. and Rosmarinus officinalis L. against antibiotic-resistant Gram-negative bacteria. Eur. J. Integr. Med. 2021; 43: 101312.

Ben El Jilali S, Beniaich G, Ihamdane R, El abdali Y, Dardour MMI, Khadmaoui A. Essential Oils of Origanum compactum: Antibacterial and Antioxidant Bioproducts. Trop. J. Nat. Prod. Res. 2023; 7(10): 4166-4170

Jemaa MB, Falleh H, Serairi R, Neves MA, Snoussi M, Isoda H, Nakajima M, Ksouri R. Nanoencapsulated Thymus capitatus essential oil as natural preservative. Innov. Food. Sci. Emerg. Technol. 2018; 45: 92-97.

Ali H, Al-Khalifa AR, Aouf A, Boukhebti H, Farouk A. Effect of nanoencapsulation on volatile constituents, and antioxidant and anticancer activities of Algerian Origanum glandulosum Desf. essential oil. Sci. Rep. 2020; 10(1): 1-9.

Sobeh M, Rezq S, Cheurfa M, Abdelfattah MA, Rashied RM, El-Shazly AM, Yasri A, Wink M, Mahmoud MF. Thymus algeriensis and Thymus fontanesii: Chemical Composition, In Vivo Antiinflammatory, Pain Killing and Antipyretic Activities: A Comprehensive Comparison. Biomol. 2020; 10(4): 599.

Quezel P, Santa S. New Flora of Algeria and Southern Desert Regions; 1963. 671p.

Abdelli I, Hassani F, Bekkel Brikci S, Ghalem S. In silico study the inhibition of angiotensin converting enzyme 2 receptor of COVID-19 by

Ammoides verticillata components harvested from Western Algeria. J Biomol. Struct Dyn. 2021; 39(9): 3263-3276.

Senouci H, Benyelles N G, Dib ME, Costa J, Muselli A. Ammoides verticillata Essential oil as Biocontrol Agent of Selected Fungi and Pest of Olive Tree. Recent Pat. Food Nutr. Agric. 2020; 11(2): 182-188.

Bekhechi C, Bekkara FA, Abdelouahid DE, Tomi F, Casanova J. Composition and Antibacterial Activity of the Essential Oil of Thymus fontanesii Boiss. et Reut. from Algeria. J. Essent. Oil Res. 2007; 19(6): 594-596.

Béjaoui A, Chaabane H, Jemli M, Boulila A, Boussaid M. Essential Oil Composition and Antibacterial Activity of Origanum vulgare subsp. glandulosum Desf. at Different Phenological Stages. J. Med. Food. 2013; 16(12): 1115-1120.

El-Jalel LF, Elkady WM, Gonaid MH, El-Gareeb KA. Difference in chemical composition and antimicrobial activity of Thymus capitatus L. essential oil at different altitudes. Futur J. Pharm. Sci. 2018; 4(2): 156-160.

Benyoucef F, Dib ME, Tabti B, Zoheir A, Costa J, Muselli A. Synergistic Effects of Essential Oils of Ammoides verticillata and Satureja candidissima Against Many Pathogenic Microorganisms. Antiinfect. Agents. 2020; 18: 72 - 78.

Adams RP. Identification of essential oil components by gas chromatography/mass spectrometry. (4th ed). Allured Publishing Corporation, Illinois; 2017. 802p.

Goyal D, Dean N, Neill S, Jones P, Dascomb K. Risk Factors for Community-Acquired Extended-Spectrum Beta-Lactamase–Producing Enterobacteriaceae Infections—A Retrospective Study of Symptomatic Urinary Tract Infections. Open Forum Infect. Dis. 2019; 6(2): 357.

CLSI. Performance Standards for Antimicrobial Susceptibility Testing. (30th ed). CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute; 2020.

Benbelaïd F, Khadir A, Abdoune MA, Bendahou M, Muselli A, Costa J. Antimicrobial activity of some essential oils against oral multidrug–resistant Enterococcus faecalis in both planktonic and biofilm state, Asian Pac. J. Trop. Biomed. 2014; 4(6): 463-472.

Zam W, Khaddour A. Anti-virulence effects of aqueous pomegranate peel extract on E. coli urinary tract infection. Prog. Nutr. 2017; 19: 98-104.

Sokhn ES, Salami A, El Roz A, Salloum L, Bahmad HF, Ghssein G. Antimicrobial Susceptibilities and Laboratory Profiles of Escherichia coli,

Klebsiella pneumoniae, and Proteus mirabilis Isolates as Agents of Urinary Tract Infection in Lebanon: Paving the Way for Better Diagnostics. Med. Sci. 2020; 8(3): 32.

De Oliveira WD, Barboza MGL, Faustino G, Inagaki WTY, Sanches MS, Kobayashi RKT, Vespero EC. Rocha SPD. Virulence, resistance and clonality of Proteus mirabilis isolated from patients with community-acquired urinary tract infection (CA-UTI) in Brazil. Microb. Pathog. 2021; 152: 104642.

Perera PDVM, Gamage S, De Silva HSM, Jayatilleke SK, de Silva N, Aydin A, Enne VI. Corea EM. Phenotypic and genotypic distribution of ESBL, AmpC β-lactamase and carbapenemase-producing Enterobacteriaceae in community-acquired and hospital-acquired urinary tract infections in Sri Lanka. J. Glob. Antimicrob. Resist. 2022; 30: 115-122.

Yandai FH, Ndoutamia G, Nadlaou B, Barro N. Prevalence and resistance profile of Escherichia coli and Klebsiella pneumoniae isolated from urinary tract infections in N'Djamena, Tchad. Int. J. Biol. Chem. Sci. 2019; 13(4): 2065-2073.

Attou A, Davenne D, Benmansour A, Lazouni HA. Chemical composition and biological activities of Ammoides verticillata essential oil from west Algeria. Phytothérapie. 2019; 17(1): 2-8.

Bendahou M, Muselli A, Grignon-Dubois M, Benyoucef M, Desjobert JM, Bernardini AF, Costa J. Antimicrobial activity and chemical composition of Origanum glandulosum Desf. essential oil and extract obtained by microwave extraction: Comparison with hydrodistillation. Food Chem. 2008; 106(1): 132-139.

Khalfi O, Sahraoui N, Bentahar F, Boutekedjiret C. Chemical composition and insecticidal properties of Origanum glandulosum (Desf.) essential oil from Algeria. J. Sci. Food. Agric. 2008; 88: 1562-1566.

Ruberto G, Baratta MT, Sari M, Kaâbeche M. Chemical composition and antioxidant activity of essential oils from Algerian Origanum glandulosum Desf. Flavour Fragr. J. 2002; 17(4): 251-254.

Belhattab R, Larous L, Figueiredo AC, Santos PA, Barroso JG, Pedro LG. Origanum glandulosum Desf. grown wild in Algeria: essential oil composition and glycosidic bound volatiles. Flavour Fragr. J. 2005; 20: 209-212.

El Mokhtar El Ouariachi JP, Bouyanzer A, Tomi P, Hammouti B, Salghi R, Majidi L, Costa J. Chemical composition and antioxidant activity of essential oils and solvent extracts of Thymus capitatus (L.) Hoffmanns and link from Morocco. J. Med. Plant Res. 2011; 5(24): 5773-5778.

Sidali L, Brada M, Fauconnier ML, Lognay G. Chemical composition and antioxidant activity of Thymus fontanesii essential oil from Algeria. Nat. Prod. J. 2020; 10(3): 193-199.

Benyoucef F, Dib MEA, Arrar Z, Costa J, Muselli A. Synergistic antioxidant activity and chemical composition of essential oils from Thymus fontanesii, Artemisia herba-alba and Rosmarinus officinalis. J. Appl. Biotechnol. Rep. 2018; 5(4): 151-156.

Dob T, Dahmane D, Benabdelkader T, Chelghoum C. Composition and Antimicrobial Activity of the Essential Oil of Thymus fontanesii. Pharm. Biol. 2006; 44(8): 607-612.

Escobar A, Perez M, Romanelli G, Blustein G. Thymol bioactivity: A review focusing on practical applications. Arab. J. Chem. 2020; 13(12): 9243-9269.

Gouyon PH, Vernet P, Guillerm JL, Valdeyron G. Polymorphisms and environment: the adaptive value of the oil polymorphisms in Thymus vulgaris L. Heredity. 1986; 57(1): 59-66.

Raina AP, Gupta V. Chemotypic characterization of diversity in essential oil composition of Ocimum species and varieties from India. J. Essent. Oil Res. 2018; 30(6): 444-456.

Tagnaout I, Zerkani H, Hadi N, El Moumen B, El Makhoukhi F, Bouhrim M, Al-Salahi R, Nasr FA, Mechchate H, Zair T. Chemical Composition, Antioxidant and Antibacterial Activities of Thymus broussonetii Boiss and Thymus capitatus (L.) Hoffmann and Link Essential Oils. Plants. 2022; 11: 954.

Suntres ZE, Coccimiglio J, Alipour M. The Bioactivity and Toxicological Actions of Carvacrol. Crit. Rev. Food Sci. Nutr. 2015; 55(3): 304-318.

Sidali L, Brada M, Fauconnier ML, Lognay G, Heuskin S. Chemical composition, acute toxicity, antimicrobial and anti-inflammatory activities of Thymus fontanesii essential oil from Algeria. Phytochem. Bioact. Subst. J. 2017; 11 (1): 11.

Loose M, Pilger E, Wagenlehner F. Anti-Bacterial Effects of Essential Oils against Uropathogenic Bacteria. Antibiotics. 2020; 9(6):358.

Jeddi M, Fikri-Benbrahim K, El Hachlafi N, Benkhaira N, Aboussemdai A, Ouaritini ZB. Chemical Composition of Thymus vulgaris, Origanum

compactum and Vetiveria zizanoides Essential oils and their Antibacterial and Antioxidant Activities. Trop. J. Nat. Prod. Res. 2023; 7(1): 2244-2250.

Fournomiti M, Kimbaris A, Mantzourani I, Plessas S, Theodoridou I, Papaemmanouil V, Kapsiotis I, Panopoulou M, Stavropoulou E, Bezirtzoglou EE, Alexopoulos A. Antimicrobial activity of essential oils of cultivated oregano (Origanum vulgare), sage (Salvia officinalis), and thyme (Thymus vulgaris) against clinical isolates of Escherichia coli, Klebsiella oxytoca, and Klebsiella pneumoniae. Microb. Ecol. Health Dis. 2015; 26(1): 23289.

Sasso MD, Culici M, Braga PC, Guffanti EE, Mucci M. Thymol: Inhibitory Activity on Escherichia coli and Staphylococcus aureus Adhesion to Human Vaginal Cells. J. Essent. Oil Res. 2006; 18(4): 455-461.

Tomičić Z, Tomičić R, Možina SS, Bucar F, Turek I, Raspor P. Antifungal and anti-adhesion activity of plant extracts and essential oils against Candida spp. and Pichia spp. J. Food Nutr. Res. 2022; 61(1): 61-68.

Alibi S, Selma WB, Mansour HB, Navas J. Activity of Essential Oils Against Multidrug-Resistant Salmonella enteritidis. Curr. Microbiol. 2022; 79(9): 273.

Šikić Pogačar M, Klančnik A, Bucar F, Langerholc T, Smole Možina S. Anti-adhesion activity of thyme (Thymus vulgaris L.) extract, thyme post-distillation waste, and olive (Olea europea L.) leaf extract against Campylobacter jejuni on polystyrene and intestine epithelial cells. J. Sci. Food Agric. 2016; 96: 2723-2730.

Mami IR, Merad-Boussalah N, Dib MEA, Tabti B, Costa J, Muselli A. Chemical Variability and Antioxidant Activities of the Essential Oils of the Aerial Parts of Ammoides verticillata and the Roots of Carthamus caeruleus and their Synergistic Effect in Combination. Comb. Chem. High Throughput Screen. 2021; 24(1): 71-78(8).

Nabet N, Boudries H, Loupassaki S, Souagui S, Madani K, Carbonell-Barrachina ÁA. Chemical composition, antimicrobial and antioxidant activities of Thymus fontanesii Boiss. et Reut. and Origanum glandulosum Desf. essential oils. Int. Food Res. J. 2017; 24(6).