Antibacterial activity of Clove Syzygium aromaticum L. and synergism with antibiotics against multidrug-resistant uropathogenic E. coli
- Autores: Marouf R.1, Ermolaev A.A.1, Podoprigora I.V.1, Senyagin A.N.1, Mbarga M.J.1
-
Afiliações:
- RUDN University
- Edição: Volume 27, Nº 3 (2023): PHYSIOLOGY
- Páginas: 379-390
- Seção: MICROBIOLOGY
- URL: https://journal-vniispk.ru/2313-0245/article/view/319710
- DOI: https://doi.org/10.22363/2313-0245-2023-27-3-379-390
- EDN: https://elibrary.ru/PZXLKU
- ID: 319710
Citar
Texto integral
Resumo
Relevance. Urinary tract infections pose a growing threat to humanity due to the rise of antibiotic resistance in uropathogens. Exploring natural sources for alternative treatments has become a prominent approach. The aim of the research was to investigate the antibacterial effects of clove (Syzygium aromaticum L.) against uropathogenic Escherichia coli (E. coli). Materials and Methods. The research was performed on three clinical multidrug-resistant uropathogenic E. coli isolates and E. coli ATCC 25922. Clove hydroalcoholic extract was obtained by cold maceration technique. To evaluate the antibacterial activity of the extract, agar well diffusion method was performed. Minimum inhibitory and minimum bactericidal concentrations of the extract were determined by microbroth dilution method. Light microscopy was used to investigate morphological changes in uropathogenic E. coli after exposure to clove extract. Checkerboard assay was used to assess synergism between clove extract and antibiotics. All obtained data were statistically processed. Results and Discussion. In well diffusion method, bacterial responses to clove extract were concentration-dependent with inhibition zone diameter of 7-10/10-15 mm for uropathogenic strains and E. coli ATCC 25922, respectively. Minimum inhibitory and minimum bactericidal concentrations of clove extract against uropathogenic strains were 25 mg/mL. The extract showed a lower minimum inhibitory concentration against E. coli ATCC 25922 (6.25 mg/ mL) with minimum bactericidal concentration being 25 mg/mL. Minimum inhibitory and minimum bactericidal concentrations ratio showed that clove extract tends to be bactericidal agent. Synergy test revealed that the combination of clove extract and nitrofurantoin or ciprofloxacin resulted in no interaction. However, minimum inhibitory concentrations of all tested agents in combinations exhibited varying degrees of decrease. Incubation of uropathogenic strains with the extract transformed them to unstable spherical L-form in percentage of 96-99 %. Conclusion. This study highlights clove as a potential natural antibacterial agent against multidrug-resistant uropathogenic E. coli, warranting further investigations into its antibacterial properties.
Sobre autores
Razan Marouf
RUDN University
Autor responsável pela correspondência
Email: razanma3rouf@gmail.com
ORCID ID: 0000-0001-9581-5381
Moscow, Russian Federation
Andrey Ermolaev
RUDN University
Email: razanma3rouf@gmail.com
ORCID ID: 0000-0001-6472-3644
Moscow, Russian Federation
Irina Podoprigora
RUDN University
Email: razanma3rouf@gmail.com
ORCID ID: 0000-0003-4099-2967
Moscow, Russian Federation
Alexander Senyagin
RUDN University
Email: razanma3rouf@gmail.com
ORCID ID: 0000-0002-4981-0149
Moscow, Russian Federation
Manga Mbarga
RUDN University
Email: razanma3rouf@gmail.com
ORCID ID: 0000-0001-9626-9247
Moscow, Russian Federation
Bibliografia
- Cortés-Rojas DF, de Souza CRF, Oliveira WP. Clove (Syzygium aromaticum): a precious spice. Asian Pac J Trop Biomed. 2014;4(2):90-96. doi: 10.1016/S2221-1691(14)60215-X.
- Pérez-Jiménez J, Neveu V, Vos F, Scalbert A. Identification of the 100 richest dietary sources of polyphenols: An application of the Phenol-Explorer database. Eur J Clin Nutr. 2010;64(3):112-120. doi: 10.1038/ejcn.2010.221.
- El-Saber Batiha G, Alkazmi LM, Wasef LG, Beshbishy AM, Nadwa EH, Rashwan EK. Syzygium aromaticum L. (Myrtaceae): Traditional Uses, Bioactive Chemical Constituents, Pharmacological and Toxicological Activities. Biomolecules. 2020;10(2):202. doi: 10.3390/biom10020202.
- Kamatou GP, Vermaak I, Viljoen AM. Eugenol - From the remote Maluku Islands to the international market place: A review of a remarkable and versatile molecule. Molecules. 2012;17(6):6953-6981. doi: 10.3390/molecules17066953.
- Vicidomini C, Roviello V, Roviello GN. Molecular Basis of the Therapeutical Potential of Clove (Syzygium aromaticum L.) and Clues to Its Anti-COVID-19 Utility. Molecules. 2021;26(7):1880. doi: 10.3390/molecules26071880.
- Han X, Parker TL. Anti-inflammatory activity of clove (Eugenia caryophyllata) essential oil in human dermal fibroblasts. Pharm Biol. 2017;55(1):1619-1622. doi: 10.1080/13880209.2017.1314513.
- Reichling J, Schnitzler P, Suschke U, Saller R. Essential oils of aromatic plants with antibacterial, antifungal, antiviral, and cytotoxic properties - An overview. Forsch Komplementarmed. 2009;16(2):79-90. doi: 10.1159/000207196.
- Fu YJ, Zu YG, Chen LY, Shi XG, Wang Z, Sun S, Efferth T. Antimicrobial activity of clove and rosemary essential oils alone and in combination. Phytotherapy Research. 2007;21(10):989-994. doi: 10.1002/ptr.2179.
- Santoro GF, Cardoso MG, Guimarães LGL, Mendonça LZ, Soares MJ. Trypanosoma cruzi: Activity of essential oils from Achillea millefolium L., Syzygium aromaticum L. and Ocimum basilicum L. on epimastigotes and trypomastigotes. Exp Parasitol. 2007;116(3):283-290. doi: 10.1016/j.exppara.2007.01.018.
- Machado M, Dinis AM, Salgueiro L, Custódio JBA, Cavaleiro C, Sousa MC. Anti-Giardia activity of Syzygium aromaticum essential oil and eugenol: Effects on growth, viability, adherence and ultrastructure. Exp Parasitol. 2011;127(4):732-739. doi: 10.1016/j.exppara.2011.01.011.
- El-kady AM, Ahmad AA, Hassan TM, El-Deek HEM, Fouad SS, Althagfan SS. Eugenol, a potential schistosomicidal agent with anti-inflammatory and antifibrotic effects against Schistosoma mansoni, induced liver pathology. Infect Drug Resist. 2019;12:709-719. doi: 10.2147/IDR.S196544.
- Kumar K, Yadav A, Srivastava S, Paswan S. Recent Trends in Indian Traditional Herbs Syzygium Aromaticum and its Health Benefits. J Pharmacogn Phytochem. 2012;1:13-22.
- Fazly Bazzaz BS, Darvishi Fork S, Ahmadi R, Khameneh B. Deep insights into urinary tract infections and effective natural remedies. African Journal of Urology. 2021;27(1):6. doi: 10.1186/s12301-020-00111-z.
- Abushaheen MA, Muzaheed, Fatani AJ, Alosaimi M, Mansy W, George M, Acharya S, Rathod S, Divakar DD, Jhugroo C, Vellappally S, Khan AA, Shaik J, Jhugroo P. Antimicrobial resistance, mechanisms and its clinical significance. Disease-a-Month. 2020;66(6):100971. doi: 10.1016/j.disamonth.2020.100971.
- Rai MK, Deshmukh SD, Ingle AP, Gade AK. Silver nanoparticles: The powerful nanoweapon against multidrug-resistant bacteria. J Appl Microbiol. 2012;112(5):841-852. doi: 10.1111/j.1365-2672.2012.05253.x.
- Anand U, Jacobo-Herrera N, Altemimi A, Lakhssassi N. A comprehensive review on medicinal plants as antimicrobial therapeutics: Potential avenues of biocompatible drug discovery. Metabolites. 2019;9(11):258. doi: 10.3390/metabo9110258.
- Najumudin K, Ayubu J, M. Elnazeer A. Antigiardial Activity of Some Plant Extracts Used in Traditional Medicine in Sudan in Comparison with Metronidazole. Microbiology: Current Research. 2018;02(04):75-82. doi: 10.35841/2591-8036.18-1025.
- Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal. 2016;6(2):71-79. doi: 10.1016/j.jpha.2015.11.005.
- Arsène MMJ, Podoprigora I V., Davares AKL, Razan M, Das MS, Senyagin AN. Antibacterial activity of grapefruit peel extracts and green-synthesized silver nanoparticles. Vet World. 2021;14(5):1330-1341. doi: 10.14202/vetworld.2021.1330-1341.
- Mouafo HT, Tchuenchieu ADK, Nguedjo MW, Edoun FLE, Tchuente BRT, Medoua GN. In vitro antimicrobial activity of Millettia laurentii De Wild and Lophira alata Banks ex C.F. Gaertn on selected foodborne pathogens associated to gastroenteritis. Heliyon. 2021;7(4): e06830. doi: 10.1016/j.heliyon.2021.e06830
- Bellio P, Fagnani L, Nazzicone L, Celenza G. New and simplified method for drug combination studies by checkerboard assay. Methods X. 2021;8:101543. doi: 10.1016/J.MEX.2021.101543.
- Celenza G, Segatore B, Setacci D, Bellio P, Brisdelli F, Piovano M, Garbarino JA, Nicoletti M, Perilli M, Amicosante G. In vitro antimicrobial activity of pannarin alone and in combination with antibiotics against methicillin-resistant Staphylococcus aureus clinical isolates. Phytomedicine. 2012;19(7):596-602. doi: 10.1016/J.PHYMED.2012.02.010.
- Gonelimali FD, Lin J, Miao W, Xuan J, Charles F, Chen M, Hatab SR. Antimicrobial Properties and Mechanism of Action of Some Plant Extracts Against Food Pathogens and Spoilage Microorganisms. Front Microbiol. 2018;9:1639. doi: 10.3389/fmicb.2018.01639.
- Oulkheir S, Aghrouch M, El Mourabit F, Dalha F, Graich H, Amouch F, Ouzaid K, Moukale A, Chadli S, Chadli Antibacterial S. Antibacterial Activity of Essential Oils Extracts from Cinnamon, Thyme, Clove and Geranium Against a Gram Negative and Gram Positive Pathogenic Bacteria. Journal of Diseases and Medicinal Plants Special Issue: New Vistas of Research in Ayurveda System of Medicine. 2017;3(1):1-5. doi: 10.11648/j.jdmp.s.2017030201.11.
- Revati S, Bipin C, Chitra PB, Minakshi B. In vitro antibacterial activity of seven Indian spices against high level gentamicin resistant strains of enterococci. Archives of Medical Science. 2015;11(4):863-868. doi: 10.5114/aoms.2015.53307
- Rosarior VL, Lim PS, Wong WK, Yue CS, Yam HC, Tan SA. Antioxidant-rich Clove Extract, A Strong Antimicrobial Agent against Urinary Tract Infections-causing Bacteria in vitro. Trop Life Sci Res. 2021;32(2):45-63. doi: 10.21315/tlsr2021.32.2.4.
- SM M, RO D, OL F. Phenolic Compounds in Antimicrobial Therapy. J Med Food. 2017;20(10):1031-1038. doi: 10.1089/JMF.2017.0017.
- Mak KK, Kamal M, Ayuba S, Sakirolla R, Kang YB, Mohandas K, Balijepalli M, Ahmad S, Pichika M. A comprehensive review on eugenol’s antimicrobial properties and industry applications: A transformation from ethnomedicine to industry. Pharmacogn Rev. 2019;13(25):1. doi: 10.4103/phrev.phrev_46_18.
- Bouarab-Chibane L, Forquet V, Lantéri P, Clément Y, Léonard-Akkari L, Oulahal N, Degraeve P, Bordes C. Antibacterial Properties of Polyphenols: Characterization and QSAR (Quantitative Structure-Activity Relationship) Models. Front Microbiol. 2019;10(APR):829. doi: 10.3389/FMICB.2019.00829
- Kothari V, Gupta A, Naraniwal M. Comparative study of various methods for extraction of antioxidant and antibacterial compounds from plant seeds. Journal of Natural Remedies. 2012;12/2:162-173. doi: 10.18311/jnr/2012/271.
- Pham H, Nguyen V, Vuong Q, Bowyer M, Scarlett C. Effect of Extraction Solvents and Drying Methods on the Physicochemical and Antioxidant Properties of Helicteres hirsuta Lour. Leaves. Technologies (Basel). 2015;3(4):285-301. doi: 10.3390/technologies3040285.
- Szakiel A, Ruszkowski D, Grudniak A, Kurek A, Wolska KI, Doligalska M, Janiszowska W. Antibacterial and antiparasitic activity of oleanolic acid and its glycosides isolated from marigold (Calendula officinalis). Planta Med. 2008;74(14):1709-1715. doi: 10.1055/s-0028-1088315.
- Kurek A, Grudniak AM, Szwed M, Klicka A, Samluk L, Wolska KI, Janiszowska W, Popowska M. Oleanolic acid and ursolic acid affect peptidoglycan metabolism in Listeria monocytogenes. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology. 2010;97(1):61-68. doi: 10.1007/s10482-009-9388-6.
- Dorota W, Marta K, Dorota TG. Effect of asiatic and ursolic acids on morphology, hydrophobicity, and adhesion of UPECs to uroepithelial cells. Folia Microbiol (Praha). 2013;58(3):245-252. doi: 10.1007/s12223-012-0205-7.
- Dörr T, Moynihan PJ, Mayer C. Bacterial Cell Wall Structure and Dynamics. Front Microbiol. 2019;10:2051. doi: 10.3389/fmicb.2019.02051.
- Sykes JE. Cell wall-deficient bacterial infections. In: Canine and Feline Infectious Diseases. W.B. Saunders; 2013:380-381. doi: 10.1016/B978-1-4377-0795-3.00039-9.
- Fabijan A, Kamruzzaman M, Martinez-Martin D, Venturini C, Mickiewicz K, Flores-Rodriguez N, Errington J, Iredell JR. L-form switching confers antibiotic, phage and stress tolerance in pathogenic Escherichia coli. bioRxiv. 2021;(10):2021.06.21.449206. doi: 10.1101/2021.06.21.449206.
- Kawai Y, Mickiewicz K, Errington J. Lysozyme Counteracts β-Lactam Antibiotics by Promoting the Emergence of L-Form Bacteria. Cell. 2018;172(5):1038-1049.e10. doi: 10.1016/J.CELL.2018.01.021.
- Glover WA, Yang Y, Zhang Y. Insights into the Molecular Basis of L-Form Formation and Survival in Escherichia coli. PLoS One. 2009;4(10):7316. doi: 10.1371/JOURNAL.PONE.0007316.
- Chikada T, Kanai T, Hayashi M, Kasai T, Oshima T, Shiomi D. Direct Observation of Conversion From Walled Cells to Wall-Deficient L-Form and Vice Versa in Escherichia coli Indicates the Essentiality of the Outer Membrane for Proliferation of L-Form Cells. Front Microbiol. 2021;12:537. doi: 10.3389/FMICB.2021.645965/BIBTEX.
- Sibanda T, Okoh A. The challenges of overcoming antibiotic resistance: Plant extracts as potential sources of antimicrobial and resistance modifying agents. Afr J Biotechnol. 2010;6(25):2886-2896. doi: 10.4314/ajb.v6i25.58241.
- Atteia HG, Hussein E. In vitro antibacterial and synergistic effects of some plant extracts against Staphylococcus aureus and Klebsiella pneumoniae. Journal of Antimicrobials. 2014;129:338-346.
- Chu CM, Lowder JL. Diagnosis and treatment of urinary tract infections across age groups. Am J Obstet Gynecol. 2018;219(1):40-51. doi: 10.1016/J.AJOG.2017.12.231.
- Uppala A, King EA, Patel D. Cefazolin versus fluoroquinolones for the treatment of community-acquired urinary tract infections in hospitalized patients. European Journal of Clinical Microbiology and Infectious Diseases. 2019;38(8):1533-1538. doi: 10.1007/S10096-019-03582-3.
- Faleiro ML, Miguel MG. Use of Essential Oils and Their Components against Multidrug-Resistant Bacteria. Fighting Multidrug Resistance with Herbal Extracts, Essential Oils and their Components. 2013:65-94. doi: 10.1016/B978-0-12-398539-2.00006-9.
- Scorzoni L, Sangalli-Leite F, de Lacorte Singulani J, de Paula e Silva ACA, Costa-Orlandi CB, Fusco-Almeida AM, Mendes-Giannini MJS. Searching new antifungals: The use of in vitro and in vivo methods for evaluation of natural compounds. J Microbiol Methods. 2016;123:68-78. doi: 10.1016/J.MIMET.2016.02.005.
- Segatore B, Bellio P, Setacci D, Brisdelli F, Piovano M, Garbarino JA, Nicoletti M, Amicosante G, Perilli M, Celenza G. In vitro interaction of usnic acid in combination with antimicrobial agents against methicillin-resistant Staphylococcus aureus clinical isolates determined by FICI and ΔE model methods. Phytomedicine. 2012;19(3-4):341-347. doi: 10.1016/J.PHYMED.2011.10.012.
- Xu X, Xu L, Yuan G, Wang Y, Qu Y, Zhou M. Synergistic combination of two antimicrobial agents closing each other’s mutant selection windows to prevent antimicrobial resistance. Sci Rep. 2018;8(1):7237. doi: 10.1038/s41598-018-25714-z.
Arquivos suplementares
