Chemical Composition and Antibacterial Effect of Clove and Thyme Essential Oils on Growth Inhibition and Biofilm Formation of Arcobacter spp. and Other Bacteria
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
39766622
PubMed Central
PMC11672449
DOI
10.3390/antibiotics13121232
PII: antibiotics13121232
Knihovny.cz E-zdroje
- Klíčová slova
- Arcobacter, antimicrobial effect, biofilm formation, clove, essential oil, thyme,
- Publikační typ
- časopisecké články MeSH
Background: In recent years, significant resistance of microorganisms to antibiotics has been observed. A biofilm is a structure that significantly aids the survival of the microbial population and also significantly affects its resistance. Methods: Thyme and clove essential oils (EOs) were subjected to chemical analysis using gas chromatography coupled to mass spectrometry (GC-MS) and gas chromatography with a flame ionization detector (GC-FID). Furthermore, the antimicrobial effect of these EOs was tested in both the liquid and vapor phases using the volatilization method. The effect of the EOs on growth parameters was monitored using an RTS-8 bioreactor. However, the effect of the EOs on the biofilm formation of commonly occurring bacteria with pathogenic potential was also monitored, but for less described and yet clinically important strains of Arcobacter spp. Results: In total, 37 and 28 compounds were identified in the thyme and clove EO samples, respectively. The most common were terpenes and also derivatives of phenolic substances. Both EOs exhibited antimicrobial activity in the liquid and/or vapor phase against at least some strains. The determined antimicrobial activity of thyme and clove oil was in the range of 32-1024 µg/mL in the liquid phase and 512-1024 µg/mL in the vapor phase, respectively. The results of the antimicrobial effect are also supported by similar conclusions from monitoring growth curves using the RTS bioreactor. The effect of EOs on biofilm formation differed between strains. Biofilm formation of Pseudomonas aeruginosa was completely suppressed in an environment with a thyme EO concentration of 1024 µg/mL. On the other hand, increased biofilm formation was found, e.g., in an environment of low concentration (1-32 µg/mL). Conclusions: The potential of using natural matrices as antimicrobials or preservatives is evident. The effect of these EOs on biofilm formation, especially Arcobacter strains, is described for the first time.
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Alvarez-Martínez F., Barrajón-Catalán E., Micol V. Tackling Antibiotic Resistance with Compounds of Natural Origin: A Comprehensive Review. Biomedicines. 2020;8:405. doi: 10.3390/biomedicines8100405. PubMed DOI PMC
Wright G. Opportunities for natural products in 21st century antibiotic discovery. Nat. Prod. Rep. 2017;34:694–701. doi: 10.1039/C7NP00019G. PubMed DOI
Chandra H., Bishnoi P., Yadav A., Patni B., Mishra A., Nautiyal A. Antimicrobial Resistance and the Alternative Resources with Special Emphasis on Plant-Based Antimicrobials—A Review. Plants. 2017;6:16. doi: 10.3390/plants6020016. PubMed DOI PMC
Shin J., Prabhakaran V., Kim K. The multi-faceted potential of plant-derived metabolites as antimicrobial agents against multidrug-resistant pathogens. Microb. Pathog. 2018;116:209–214. doi: 10.1016/j.micpath.2018.01.043. PubMed DOI
Sharma S., Mohler J., Mahajan S., Schwartz S., Bruggemann L., Aalinkeel R. Microbial Biofilm: A Review on Formation, Infection, Antibiotic Resistance, Control Measures, and Innovative Treatment. Microorganisms. 2023;11:1614. doi: 10.3390/microorganisms11061614. PubMed DOI PMC
Sadekuzzaman M., Yang S., Mizan M., Ha S. Current and Recent Advanced Strategies for Combating Biofilms. Compr. Rev. Food Sci. Food Saf. 2015;14:491–509. doi: 10.1111/1541-4337.12144. DOI
Vestby L., Gronseth T., Simm R., Nesse L. Bacterial Biofilm and its Role in the Pathogenesis of Disease. Antibiotics. 2020;9:59. doi: 10.3390/antibiotics9020059. PubMed DOI PMC
Abdallah E., Alhatlani B., Menezes R., Martins C. Back to Nature: Medicinal Plants as Promising Sources for Antibacterial Drugs in the Post-Antibiotic Era. Plants. 2023;12:3077. doi: 10.3390/plants12173077. PubMed DOI PMC
Pancu D., Scurtu A., Macasoi I., Marti D., Mioc M., Soica C., Coricovac D., Horhat D., Poenaru M., Dehelean C. Antibiotics: Conventional Therapy and Natural Compounds with Antibacterial Activity—A Pharmaco-Toxicological Screening. Antibiotics. 2021;10:401. doi: 10.3390/antibiotics10040401. PubMed DOI PMC
Khameneh B., Iranshahy M., Soheili V., Bazzaz B. Review on plant antimicrobials: A mechanistic viewpoint. Antimicrob. Resist. Infect. Control. 2019;8:118. doi: 10.1186/s13756-019-0559-6. PubMed DOI PMC
Mutlu-Ingok A., Catalkaya G., Capanoglu E., Karbancioglu-Guler F. Antioxidant and antimicrobial activities of fennel, ginger, oregano and thyme essential oils. Food Front. 2021;2:508–518. doi: 10.1002/fft2.77. DOI
Kowalczyk A., Przychodna M., Sopata S., Bodalska A., Fecka I. Thymol and Thyme Essential Oil-New Insights into Selected Therapeutic Applications. Molecules. 2020;25:4125. doi: 10.3390/molecules25184125. PubMed DOI PMC
Banerjee K., Madhyastha H., Sandur V., Manikandanath N., Thiagarajan N., Thiagarajan P. Anti-inflammatory and wound healing potential of a clove oil emulsion. Colloids Surf. B Biointerfaces. 2020;193:111102. doi: 10.1016/j.colsurfb.2020.111102. PubMed DOI
Collado L., Figueras M.J. Taxonomy, Epidemiology, and Clinical Relevance of the Genus Arcobacter. Clin. Microbiol. Rev. 2011;24:174–192. doi: 10.1128/CMR.00034-10. PubMed DOI PMC
Kabeya H., Maruyama S., Morita Y., Ohsuga T., Ozawa S. Prevalence of Arcobacter species in retail meats and antimicrobial susceptibility of the isolates in Japan. Int. J. Food Microbiol. 2004;90:303–308. doi: 10.1016/S0168-1605(03)00322-2. PubMed DOI
Shrestha R., Tanaka Y., Haramoto E. A Review on the Prevalence of Arcobacter in Aquatic Environments. Water. 2022;14:1266. doi: 10.3390/w14081266. DOI
Zautner A.E., Riedel T., Bunk B., Spröer C., Boahen K.G. Molecular characterization of Arcobacter butzleri isolates from poultry in rural Ghana. Front. Cell. Infect. Microbiol. 2023;13:1094067. doi: 10.3389/fcimb.2023.1094067. PubMed DOI PMC
Van den Abeele A.M., Vogelaers D., Van Hende J., Houf K. Prevalence of Arcobacter Species among Humans, Belgium, 2008–2013. Emerg. Infect. Dis. 2014;20:1731–1734. doi: 10.3201/eid2010.140433. PubMed DOI PMC
Miller W.G., Parker C.T., Rubenfield M., Mendz G.L., Wösten M.M.S.M. The Complete Genome Sequence and Analysis of the Epsilonproteobacterium Arcobacter butzleri. PLoS ONE. 2007;12:e1358. doi: 10.1371/journal.pone.0001358. PubMed DOI PMC
Silha D., Moravkova K., Skodova G., Vytrasova J. Viability and biofilm formation of Arcobacter spp. at various processing temperatures. Food Nutr. Res. 2019;58:208–213.
Silha D., Sirotkova S., Svarcova K., Hofmeisterova L., Korycanova K., Silhova L. Biofilm Formation Ability of Arcobacter-like and Campylobacter Strains under Different Conditions and on Food Processing Materials. Microorganisms. 2021;9:2017. doi: 10.3390/microorganisms9102017. PubMed DOI PMC
Svarcova K., Pejchalova M., Silha D. The Effect of Antibiotics on Planktonic Cells and Biofilm Formation Ability of Collected Arcobacter-like Strains and Strains Isolated within the Czech Republic. Antibiotics. 2022;11:87. doi: 10.3390/antibiotics11010087. PubMed DOI PMC
Ferreira S., Luís Â., Oleastro M., Pereira L., Domingues F.C. A meta-analytic perspective on Arcobacter spp. antibiotic resistance. J. Glob. Antimicrob. Resist. 2019;16:130–139. doi: 10.1016/j.jgar.2018.12.018. PubMed DOI
Gabucci C., Baldelli G., Amagliani G., Schiavano G.F., Savelli D. Widespread Multidrug Resistance of Arcobacter butzleri Isolated from Clinical and Food Sources in Central Italy. Antibiotics. 2023;12:1292. doi: 10.3390/antibiotics12081292. PubMed DOI PMC
Vicente-Martins S., Oleastro M., Domingues F.C., Ferreira S. Arcobacter spp. at retail food from Portugal: Prevalence, genotyping and antibiotics resistance. Food Control. 2018;85:107–112. doi: 10.1016/j.foodcont.2017.09.024. DOI
Ciortino S., Arculeo P., Alio V., Cardamone C., Nicastro L. Occurrence and Antimicrobial Resistance of Arcobacter spp. Recovered from Aquatic Environments. Antibiotics. 2021;10:288. doi: 10.3390/antibiotics10030288. PubMed DOI PMC
Martinez-Malaxetxebarria I., Girbau C., Salazar-Sánchez A., Baztarrika I., Martínez-BallesTeros I. Genetic characterization and biofilm formation of potentially pathogenic foodborne Arcobacter isolates. Int. J. Food Microbiol. 2022;373:109712. doi: 10.1016/j.ijfoodmicro.2022.109712. PubMed DOI
Salazar-Sánchez A., Baztarrika I., Alonso R., Fernández-Astorga A., Martínez-Ballesteros I. Arcobacter butzleri Biofilms: Insights into the Genes Beneath Their Formation. Microorganisms. 2022;10:1280. doi: 10.3390/microorganisms10071280. PubMed DOI PMC
Laird K., Phillips C. Vapour phase: A potential future use for essential oils as antimicrobials? Lett. Appl. Microbiol. 2012;54:169–174. doi: 10.1111/j.1472-765X.2011.03190.x. PubMed DOI
Acs K., Bencsik T., Böszörményi A., Kocsis B., Horváth G. Essential Oils and Their Vapors as Potential Antibacterial Agents against Respiratory Tract Pathogens. Nat. Prod. Commun. 2016;11:1709–1712. PubMed
Amat S., Baines D., Alexander T. A vapour phase assay for evaluating the antimicrobial activities of essential oils against bovine respiratory bacterial pathogens. Lett. Appl. Microbiol. 2017;65:489–495. doi: 10.1111/lam.12804. PubMed DOI
Feyaerts A., Mathé L., Luyten W., Tournu H., Van Dyck K., Broekx L., Van Dijck P. Assay and recommendations for the detection of vapour-phase-mediated antimicrobial activities. Flavour Fragr. J. 2017;32:347–353. doi: 10.1002/ffj.3400. DOI
Houdkova M., Doskocil I., Urbanova K., Tulin E., Rondevaldova J., Tulin A., Kudera T., Tulin E., Zeleny V., Kokoska L. Evaluation of Antipneumonic Effect of Philippine Essential Oils Using Broth Microdilution Volatilization Method and Their Lung Fibroblasts Toxicity. Nat. Prod. Commun. 2018;13:1059–1066. doi: 10.1177/1934578X1801300834. DOI
Reyes-Jurado F., Cervantes-Rincón T., Bach H., López-Malo A., Palou E. Antimicrobial activity of Mexican oregano (Lippia berlandieri), thyme (Thymus vulgaris), and mustard (Brassica nigra) essential oils in gaseous phase. Ind. Crops Prod. 2019;131:90–95. doi: 10.1016/j.indcrop.2019.01.036. DOI
Santomauro F., Donato R., Pini G., Sacco C., Ascrizzi R., Bilia A. Liquid and Vapor-Phase Activity of Artemisia annua Essential Oil against Pathogenic Malassezia spp. Planta Med. 2018;84:160–167. doi: 10.1055/s-0043-118912. PubMed DOI
Torpol K., Wiriyacharee P., Sriwattana S., Sangsuwan J., Prinyawiwatkul W. Antimicrobia activity of garlic (Allium sativum L.) and holy basil (Ocimum sanctum L.) essential oils applied by liquid vs. vapour phases. J. Food Sci. Technol. 2018;53:2119–2128. doi: 10.1111/ijfs.13799. DOI
Chroho M., Rouphael Y., Petropoulos S., Bouissane L. Carvacrol and Thymol Content Affects the Antioxidant and Antibacterial Activity of Origanum compactum and Thymus zygis Essential Oils. Antibiotics. 2024;13:139. doi: 10.3390/antibiotics13020139. PubMed DOI PMC
Botelho M.A., Nogueira N.A.P., Bastos G.M., Fonseca S.G.C., Lemos T.L.G. Antimicrobial activity of the essential oil from Lippia sidoides, carvacrol and thymol against oral pathogens. Braz. J. Med. Biol. Res. 2007;40:349–356. doi: 10.1590/S0100-879X2007000300010. PubMed DOI
Xu J., Zhou F., Ji B.-P., Pei R.-S., Xu N. The antibacterial mechanism of carvacrol and thymol against Escherichia coli. Lett. Appl. Microbiol. 2008;47:174–179. doi: 10.1111/j.1472-765X.2008.02407.x. PubMed DOI
Kachur K., Suntres Z. The antibacterial properties of phenolic isomers, carvacrol and thymol. Crit. Rev. Food Sci. Nutr. 2020;60:3042–3053. doi: 10.1080/10408398.2019.1675585. PubMed DOI
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. 2015;6:165. doi: 10.3389/fmicb.2015.00165. PubMed DOI PMC
Hajibonabi A., Yekani M., Sharifi S., Nahad J.S., Dizaj S.M. Antimicrobial activity of nanoformulations of carvacrol and thymol: New trend and applications. OpenNano. 2023;13:100170. doi: 10.1016/j.onano.2023.100170. DOI
De Lisi A., Tedone L., Montesano V., Sarli G., Negro D. Chemical characterisation of Thymus populations belonging from Southern Italy. Food Chem. 2011;125:1284–1286. doi: 10.1016/j.foodchem.2010.10.011. DOI
Pirbalouti A., Hashemi M., Ghahfarokhi F. Essential oil and chemical compositions of wild and cultivated Thymus daenensis Celak and Thymus vulgaris L. Ind. Crops Prod. 2013;48:43–48. doi: 10.1016/j.indcrop.2013.04.004. DOI
Rota M., Herrera A., Martínez R., Sotomayor J., Jordán M. Antimicrobial activity and chemical composition of Thymus vulgaris, Thymus zygis and Thymus hyemalis essential oils. Food Control. 2008;19:681–687. doi: 10.1016/j.foodcont.2007.07.007. DOI
Satyal P., Murray B., McFeeters R., Setzer W. Essential Oil Characterization of Thymus vulgaris from Various Geographical Locations. Foods. 2016;5:70. doi: 10.3390/foods5040070. PubMed DOI PMC
Chbel A., Elmakssoudi A., Rey-Méndez M., Barja J., Filali O., Soukri A., El Khalfi B. Comparative Study of Essential Oil Composition, Anti-bacterial And Antioxidant Activities of the Aerial Parts of Thymus vulgaris Grown in Morocco and France. J. Essent. Oil Bear. Plants. 2022;25:380–392. doi: 10.1080/0972060X.2022.2077141. DOI
Kim M., Sowndhararajan K., Kim S. The Chemical Composition and Biological Activities of Essential Oil from Korean Native Thyme Bak-Ri-Hyang (Thymus quinquecostatus Celak.) Molecules. 2022;27:4251. doi: 10.3390/molecules27134251. PubMed DOI PMC
Yesil-Celiktas O., Kocabas E., Bedir E., Sukan F., Ozek T., Baser K. Antimicrobial activities of methanol extracts and essential oils of Rosmarinus officinalis, depending on location and seasonal variations. Food Chem. 2007;100:553–559. doi: 10.1016/j.foodchem.2005.10.011. DOI
Napoli E., Curcuruto G., Ruberto G. Screening of the essential oil composition of wild Sicilian thyme. Biochem. Syst. Ecol. 2010;38:816–822. doi: 10.1016/j.bse.2010.08.008. DOI
Amiri H. Essential Oils Composition and Antioxidant Properties of Three Thymus Species. Evid.-Based Complement. Altern. Med. 2012;2012:728065. doi: 10.1155/2012/728065. PubMed DOI PMC
Hudaib M., Speroni E., Di Pietra A., Cavrini V. GC/MS evaluation of thyme (Thymus vulgaris L.) oil composition and variations during the vegetative cycle. J. Pharm. Biomed. Anal. 2002;29:691–700. doi: 10.1016/S0731-7085(02)00119-X. PubMed DOI
Zeljkovic S., Smékalová K., Kaffková K., Stefelová N. Influence of post-harvesting period on quality of thyme and spearmint essential oils. J. Appl. Res. Med. Aromat. Plants. 2021;25:100335.
Baranauskiené R., Venskutonis P., Viskelis P., Dambrauskiené E. Influence of nitrogen fertilizers on the yield and composition of thyme (Thymus vulgaris) J. Agric. Food Chem. 2003;51:7751–7758. doi: 10.1021/jf0303316. PubMed DOI
Bolechowski A., Moral R., Bustamante M., Bartual J., Paredes C., Perez-Murcia M., Carbonell-Barrachina A. Winery-distillery composts as partial substitutes of traditional growing media: Effect on the volatile composition of thyme essential oils. Sci. Hortic. 2015;193:69–76. doi: 10.1016/j.scienta.2015.07.001. DOI
Jirovetz L., Buchbauer G., Stoilova I., Stoyanova A., Krastanov A., Schmidt E. Chemical composition and antioxidant properties of clove leaf essential oil. J. Agric. Food Chem. 2006;54:6303–6307. doi: 10.1021/jf060608c. PubMed DOI
Amelia B., Saepudin E., Cahyana A., Rahayu D., Sulistyoningrum A., Haib J. GC-MS Analysis of Clove (Syzygium aromaticum) Bud Essential Oil from Java and Manado. AIP Conf. Proc. 2017;1862:030082.
Kiki M. In Vitro Antiviral Potential, Antioxidant, and Chemical Composition of Clove (Syzygium aromaticum) Essential Oil. Molecules. 2023;28:2421. doi: 10.3390/molecules28062421. PubMed DOI PMC
Xu J., Liu T., Hu Q., Cao X. Chemical Composition, Antibacterial Properties and Mechanism of Action of Essential Oil from Clove Buds against Staphylococcus aureus. Molecules. 2016;21:1194. doi: 10.3390/molecules21091194. PubMed DOI PMC
Devi K.P., Nisha S.A., Sakthivel R., Pandian S.K. Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. J. Ethnopharmacol. 2010;130:107–115. doi: 10.1016/j.jep.2010.04.025. PubMed DOI
Filgueiras C.T., Vanetti M.C.D. Effect of eugenol on growth and listeriolysin o production by Listeria monocytogenes. Braz. Arch. Biol. Technol. 2006;49:405–409. doi: 10.1590/S1516-89132006000400008. DOI
Walsh S.E., Maillard J.-Y., Russell A.D., Catrenich C.E., Charbonneau D.L. Activity and mechanisms of action of selected biocidal agents on Gram-positive and -negative bacteria. J. Appl. Microbiol. 2003;94:240–247. doi: 10.1046/j.1365-2672.2003.01825.x. PubMed DOI
Gill A.O., Holley R.A. Disruption of Escherichia coli, Listeria monocytogenes and Lactobacillus sakei cellular membranes by plant oil aromatics. Int. J. Food Microbiol. 2006;108:1–9. doi: 10.1016/j.ijfoodmicro.2005.10.009. PubMed DOI
Burt S. Essential oils: Their antibacterial properties and potential applications in foods—A review. Int. J. Food Microbiol. 2004;94:223–253. doi: 10.1016/j.ijfoodmicro.2004.03.022. PubMed DOI
Sabzikar A., Hosseinihashemi S., Shirmohammadli Y., Jalaligoldeh A. Chemical Composition and Antimicrobial Activity of Extracts from Thyme and Rosemary Against Staphylococcus aureus and Candida albicans. Bioresources. 2020;15:9656–9671. doi: 10.15376/biores.15.4.9656-9671. DOI
Vassiliou E., Awoleye O., Davis A., Mishra S. Anti-Inflammatory and Antimicrobial Properties of Thyme Oil and Its Main Constituents. Int. J. Mol. Sci. 2023;24:6936. doi: 10.3390/ijms24086936. PubMed DOI PMC
Xiao S., Cui P., Shi W., Zhang Y. Identification of essential oils with activity against stationary phase Staphylococcus aureus. BMC Complement. Med. Ther. 2020;20:99. doi: 10.1186/s12906-020-02898-4. PubMed DOI PMC
Lasek-Nesselquist E., Lug J., Schneiders R., Ma Z., Russo V., Mishra S., Pai M., Pata J., McDonough K., Malik M. Insights Into the Evolution of Staphylococcus aureus Daptomycin Resistance From an in vitro Bioreactor Model. Front. Microbiol. 2019;10:345. doi: 10.3389/fmicb.2019.00345. PubMed DOI PMC
Oussalah M., Caillet S., Saucier L., Lacroix M. Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E-coli O157:H7, Salmonella Typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control. 2007;18:414–420. doi: 10.1016/j.foodcont.2005.11.009. DOI
Beno F., Velková A., Hruska F., Sevcik R. Use of Lactoperoxidase Inhibitory Effects to Extend the Shelf Life of Meat and Meat Products. Microorganisms. 2024;12:1010. doi: 10.3390/microorganisms12051010. PubMed DOI PMC
Fu Y., Chen L., Zu Y., Liu Z., Liu X., Yao L., Efferth T. The Antibacterial Activity of Clove Essential Oil Against Propionibacterium acnes and Its Mechanism of Action. Arch. Dermatol. 2009;145:86–88. doi: 10.1001/archdermatol.2008.549. PubMed DOI
Kaur M., Sharma S., Kalia A., Sandhu N. Essential oils and their blends: Mechanism of antibacterial activity and antibiofilm potential on food-grade maize starch packaging films. Int. Microbiol. 2024;27:1707–1724. doi: 10.1007/s10123-024-00514-w. PubMed DOI
Pandey V., Shams R., Singh R., Dar A., Pandiselvam R., Rusu A., Trif M. A comprehensive review on clove (Caryophyllus aromaticus L.) essential oil and its significance in the formulation of edible coatings for potential food applications. Front. Nutr. 2022;9:987674. PubMed PMC
Siddiqua S., Anusha B., Ashwini L., Negi P. Antibacterial activity of cinnamaldehyde and clove oil: Effect on selected foodborne pathogens in model food systems and watermelon juice. J. Food Sci. Technol. 2015;52:5834–5841. doi: 10.1007/s13197-014-1642-x. PubMed DOI PMC
Sun H., Luo D., Zheng S., Li Z., Xu W. Antimicrobial behavior and mechanism of clove oil nanoemulsion. J. Food Sci. Technol. 2022;59:1939–1947. doi: 10.1007/s13197-021-05208-z. PubMed DOI PMC
Nazzaro F., Fratianni F., De Martino L., Coppola R., De Feo V. Effect of Essential Oils on Pathogenic Bacteria. Pharmaceuticals. 2013;6:1451–1474. doi: 10.3390/ph6121451. PubMed DOI PMC
Trombetta D., Castelli F., Sarpietro M., Venuti V., Cristani M., Daniele C., Saija A., Mazzanti G., Bisignano G. Mechanisms of antibacterial action of three monoterpenes. Antimicrob. Agents Chemother. 2005;49:2474–2478. doi: 10.1128/AAC.49.6.2474-2478.2005. PubMed DOI PMC
Bai J., Li J., Chen Z., Bai X., Yang Z., Wang Z., Yang Y. Antibacterial activity and mechanism of clove essential oil against foodborne pathogens. LWT Food Sci. Technol. 2023;173:114249. doi: 10.1016/j.lwt.2022.114249. DOI
Alanazi A., Alqasmi M., Alrouji M., Kuriri F., Almuhanna Y., Joseph B., Asad M. Antibacterial Activity of Syzygium aromaticum (Clove) Bud Oil and Its Interaction with Imipenem in Controlling Wound Infections in Rats Caused by Methicillin-Resistant Staphylococcus aureus. Molecules. 2022;27:8551. doi: 10.3390/molecules27238551. PubMed DOI PMC
Gurbuz M., Korkmaz B. The anti-campylobacter activity of eugenol and its potential for poultry meat safety: A review. Food Chem. 2022;394:133519. doi: 10.1016/j.foodchem.2022.133519. PubMed DOI
Taleuzzaman M., Jain P., Verma R., Iqbal Z., Mirza M. Eugenol as a Potential Drug Candidate: A Review. Curr. Top. Med. Chem. 2021;21:1804–1815. doi: 10.2174/1568026621666210701141433. PubMed DOI
Houdkova M., Rondevaldova J., Doskocil I., Kokoska L. Evaluation of antibacterial potential and toxicity of plant volatile compounds using new broth microdilution volatilization method and modified MTT assay. Fitoterapia. 2017;118:56–62. doi: 10.1016/j.fitote.2017.02.008. PubMed DOI
Rebickova K., Bajer T., Silha D., Houdkova M., Ventura K., Bajerova P. Chemical Composition and Determination of the Antibacterial Activity of Essential Oils in Liquid and Vapor Phases Extracted from Two Different Southeast Asian Herbs-Houttuynia cordata (Saururaceae) and Persicaria odorata (Polygonaceae) Molecules. 2020;25:2432. doi: 10.3390/molecules25102432. PubMed DOI PMC
Sateriale D., Forgione G., De Cristofaro G., Pagliuca C., Colicchio R., Salvatore P., Paolucci M., Pagliarulo C. Antibacterial and Antibiofilm Efficacy of Thyme (Thymus vulgaris L.) Essential Oil against Foodborne Illness Pathogens, Salmonella enterica subsp. enterica Serovar Typhimurium and Bacillus cereus. Antibiotics. 2023;12:485. doi: 10.3390/antibiotics12030485. PubMed DOI PMC
Solomakos N., Govaris A., Koidis P., Botsoglou N. The antimicrobial effect of thyme essential oil, nisin and their combination against Escherichia coli O157:H7 in minced beef during refrigerated storage. Meat Sci. 2008;80:159–166. doi: 10.1016/j.meatsci.2007.11.014. PubMed DOI
Xue J., Davidson P., Zhong Q. Antimicrobial activity of thyme oil co-nanoemulsified with sodium caseinate and lecithin. Int. J. Food Microbiol. 2015;210:1–8. doi: 10.1016/j.ijfoodmicro.2015.06.003. PubMed DOI
Marchese A., Orhan I., Daglia M., Barbieri R., Di Lorenzo A., Nabavi S., Gortzi O., Izadi M., Nabavi S. Antibacterial and antifungal activities of thymol: A brief review of the literature. Food Chem. 2016;210:402–414. doi: 10.1016/j.foodchem.2016.04.111. PubMed DOI
Bonetti A., Tugnoli B., Piva A., Grilli E. Thymol as an Adjuvant to Restore Antibiotic Efficacy and Reduce Antimicrobial Resistance and Virulence Gene Expression in Enterotoxigenic Escherichia coli Strains. Antibiotics. 2022;11:1073. doi: 10.3390/antibiotics11081073. PubMed DOI PMC
Fisher K., Rowe C., Phillips C.A. The survival of three strains of Arcobacter butzleri in the presence of lemon, orange and bergamot essential oils and their components in vitro and on food. Lett. Appl. Microbiol. 2007;44:495–499. doi: 10.1111/j.1472-765X.2006.02106.x. PubMed DOI
Horváth G., Ács K. Essential oils in the treatment of respiratory tract diseases highlighting their role in bacterial infections and their anti-inflammatory action: A review. Flavour Fragr. J. 2015;30:331–341. doi: 10.1002/ffj.3252. PubMed DOI PMC
Doran A.L., Morden W.E., Dunn K., Edwards-Jones V. Vapour-phase activities of essential oils against antibiotic sensitive and resistant bacteria including MRSA. Lett. Appl. Microbiol. 2009;48:387–392. doi: 10.1111/j.1472-765X.2009.02552.x. PubMed DOI
Fancello F., Petretto G.L., Marceddu S., Venditti T., Pintore G. Antimicrobial activity of gaseous Citrus limon var pompia leaf essential oil against Listeria monocytogenes on ricotta salata cheese. Food Microbiol. 2020;87:103386. doi: 10.1016/j.fm.2019.103386. PubMed DOI
López P., Sánchez C., Batlle R., Nerín C. Solid- and Vapor-Phase Antimicrobial Activities of Six Essential Oils: Susceptibility of Selected Foodborne Bacterial and Fungal Strains. J. Agric. Food Chem. 2005;53:6939–6946. doi: 10.1021/jf050709v. PubMed DOI
López P., Sánchez C., Batlle R., Nerín C. Vapor-Phase Activities of Cinnamon, Thyme, and Oregano Essential Oils and Key Constituents against Foodborne Microorganisms. J. Agric. Food Chem. 2007;55:4348–4356. doi: 10.1021/jf063295u. PubMed DOI
López P., Sánchez C., Batlle R., Nerín C. Development of Flexible Antimicrobial Films Using Essential Oils as Active Agents. J. Agric. Food Chem. 2007;55:8814–8824. doi: 10.1021/jf071737b. PubMed DOI
Rodríguez A., Batlle R., Nerín C. The use of natural essential oils as antimicrobial solutions in paper packaging. Part II. Prog. Org. Coat. 2007;60:33–38. doi: 10.1016/j.porgcoat.2007.06.006. DOI
Das M., Roy S., Guha C., Saha A., Singh M. In vitro evaluation of antioxidant and antibacterial properties of supercritical CO2 extracted essential oil from clove bud (Syzygium aromaticum) J. Plant Biochem. Biotechnol. 2021;30:387–391. doi: 10.1007/s13562-020-00566-9. DOI
Mousavi F., Gionfriddo E., Carasek E., Souza-Silva E., Pawliszyn J. Coupling solid phase microextraction to complementary separation platforms for metabotyping of E. coli metabolome in response to natural antibacterial agents. Metabolomics. 2016;12:169. doi: 10.1007/s11306-016-1111-9. DOI
Ghazvinian M., Marghmalek S., Gholami M., Gholami S., Amiri E., Goli H. Antimicrobial resistance patterns, virulence genes, and biofilm formation in enterococci strains collected from different sources. BMC Infect. Dis. 2024;24:274. doi: 10.1186/s12879-024-09117-2. PubMed DOI PMC
Nourbakhsh F., Nasrollahzadeh M., Tajani A., Soheili V., Hadizadeh F. Bacterial biofilms and their resistance mechanisms: A brief look at treatment with natural agents. Folia Microbiol. 2022;67:535–554. doi: 10.1007/s12223-022-00955-8. PubMed DOI
Pai L., Patil S., Liu S., Wen F. A growing battlefield in the war against biofilm-induced antimicrobial resistance: Insights from reviews on antibiotic resistance. Front. Cell. Infect. Microbiol. 2023;13:1327069. doi: 10.3389/fcimb.2023.1327069. PubMed DOI PMC
Rather M., Gupta K., Mandal M. Microbial biofilm: Formation, architecture, antibiotic resistance, and control strategies. Braz. J. Microbiol. 2021;52:1701–1718. doi: 10.1007/s42770-021-00624-x. PubMed DOI PMC
Srinivasan R., Santhakumari S., Poonguzhali P., Geetha M., Dyavaiah M., Lin X. Bacterial Biofilm Inhibition: A Focused Review on Recent Therapeutic Strategies for Combating the Biofilm Mediated Infections. Front. Microbiol. 2021;12:676458. doi: 10.3389/fmicb.2021.676458. PubMed DOI PMC
Dsouza F., Dinesh S., Sharma S. Understanding the intricacies of microbial biofilm formation and its endurance in chronic infections: A key to advancing biofilm-targeted therapeutic strategies. Arch. Microbiol. 2024;206:85. doi: 10.1007/s00203-023-03802-7. PubMed DOI
Li X., Gu N., Huang T., Zhong F., Peng G. Pseudomonas aeruginosa: A typical biofilm forming pathogen and an emerging but underestimated pathogen in food processing. Front. Microbiol. 2023;13:1114199. doi: 10.3389/fmicb.2022.1114199. PubMed DOI PMC
Vani S., Vadakkan K., Mani B. A narrative review on bacterial biofilm: Its formation, clinical aspects and inhibition strategies. Future J. Pharm. Sci. 2023;9:50. doi: 10.1186/s43094-023-00499-9. DOI
Silha D., Svarcova K., Bajer T., Kralovec K., Tesarova E., Mouckova K., Pejchalova M., Bajerova P. Chemical Composition of Natural Hydrolates and Their Antimicrobial Activity on Arcobacter-like Cells in Comparison with Other Microorganisms. Molecules. 2020;25:5654. doi: 10.3390/molecules25235654. PubMed DOI PMC
Artini M., Patsilinakos A., Papa R., Bozovic M., Sabatino M., Garzoli S., Vrenna G., Tilotta M., Pepi F., Ragno R., et al. Antimicrobial and Antibiofilm Activity and Machine Learning Classification Analysis of Essential Oils from Different Mediterranean Plants against Pseudomonas aeruginosa. Molecules. 2018;23:482. doi: 10.3390/molecules23020482. PubMed DOI PMC
Papa R., Garzoli S., Vrenna G., Sabatino M., Sapienza F., Relucenti M., Donfrancesco O., Fiscarelli E., Artini M., Selan L., et al. Essential Oils Biofilm Modulation Activity, Chemical and Machine Learning Analysis. Application on Staphylococcus aureus Isolates from Cystic Fibrosis Patients. Int. J. Mol. Sci. 2020;21:9258. doi: 10.3390/ijms21239258. PubMed DOI PMC
Elumalai P., Gao X., Cui J., Kumar A.S., Dhandapani P. Biofilm formation, occurrence, microbial communication, impact and characterization methods in natural and anthropic systems: A review. Environ. Chem. Lett. 2024;22:1297–1326. doi: 10.1007/s10311-024-01715-5. DOI
kathariosKatharios-Lanwermeyer S., Koval S.A., Barrack K.E., O’toole G.A., Galperin M.Y. The Diguanylate Cyclase YfiN of Pseudomonas aeruginosa Regulates Biofilm Maintenance in Response to Peroxide. J. Bacteriol. 2022;204:00396-21. doi: 10.1128/JB.00396-21. PubMed DOI PMC
Silva E., Teixeira J.A., Pereira M.O., Rocha C.M.R., Sousa A.M. Evolving biofilm inhibition and eradication in clinical settings through plant-based antibiofilm agents. Phytomedicine. 2023;119:154973. doi: 10.1016/j.phymed.2023.154973. PubMed DOI
Wang X., Liu M., Yu C., Li J., Zhou X. Biofilm formation: Mechanistic insights and therapeutic targets. Mol. Biomed. 2023;4:49. doi: 10.1186/s43556-023-00164-w. PubMed DOI PMC
Nostro A., Roccaro A., Bisignano G., Marino A., Cannatelli M., Pizzimenti F., Cioni P., Procopio F., Blanco A. Effects of oregano, carvacrol and thymol on Staphylococcus aureus and Staphylococcus epidermidis biofilms. J. Med. Microbiol. 2007;56:519–523. doi: 10.1099/jmm.0.46804-0. PubMed DOI
Nuryastuti T., Van der Mei H.C., Busscher H.J., Iravati S., Aman A.T. Effect of Cinnamon Oil on icaA Expression and Biofilm Formation by Staphylococcus epidermidis. Appl. Environ. Microbiol. 2009;75:6850–6855. doi: 10.1128/AEM.00875-09. PubMed DOI PMC
Ben Abdallah F., Lagha R., Gaber A. Biofilm Inhibition and Eradication Properties of Medicinal Plant Essential Oils against Methicillin-Resistant Staphylococcus aureus Clinical Isolates. Pharmaceuticals. 2020;13:369. doi: 10.3390/ph13110369. PubMed DOI PMC
Nuta D., Limban C., Chirita C., Chifiriuc M., Costea T., Ionita P., Nicolau I., Zarafu I. Contribution of Essential Oils to the Fight against Microbial Biofilms—A Review. Processes. 2021;9:537. doi: 10.3390/pr9030537. DOI
Martinez A., Manrique-Moreno M., Klaiss-Luna M., Stashenko E., Zafra G., Ortiz C. Effect of Essential Oils on Growth Inhibition, Biofilm Formation and Membrane Integrity of Escherichia coli and Staphylococcus aureus. Antibiotics. 2021;10:1474. doi: 10.3390/antibiotics10121474. PubMed DOI PMC
Melo R., Azevedo A., Pereira A., Rocha R., Cavalcante R., Matos M., Lopes P., Gomes G., Rodrigues T., dos Santos H., et al. Chemical Composition and Antimicrobial Effectiveness of Ocimum gratissimum L. Essential Oil Against Multidrug-Resistant Isolates of Staphylococcus aureus and Escherichia coli. Molecules. 2019;24:3864. doi: 10.3390/molecules24213864. PubMed DOI PMC
Budzynska A., Wieckowska-Szakiel M., Sadowska B., Kalemba D., Rózalska B. Antibiofilm Activity of Selected Plant Essential Oils and their Major Components. Pol. J. Microbiol. 2011;60:35–41. doi: 10.33073/pjm-2011-005. PubMed DOI
Wijesundara N., Rupasinghe H. Essential oils from Origanum vulgare and Salvia officinalis exhibit antibacterial and anti-biofilm activities against Streptococcus pyogenes. Microb. Pathog. 2018;117:118–127. doi: 10.1016/j.micpath.2018.02.026. PubMed DOI
Chmit M., Kanaan H., Habib J., Abbass M., Mcheik A., Chokr A. Antibacterial and antibiofilm activities of polysaccharides, essential oil, and fatty oil extracted from Laurus nobilis growing in Lebanon. Asian Pac. J. Trop. Med. 2014;7:S546–S552. doi: 10.1016/S1995-7645(14)60288-1. PubMed DOI
Millezi A., Cardoso M., Alves E., Piccoli R. Reduction of Aeromonas hidrophyla biofilm on stainless stell surface by essential oils. Braz. J. Microbiol. 2013;44:73–80. doi: 10.1590/S1517-83822013005000015. PubMed DOI PMC
Benzaid C., Belmadani A., Djeribi R., Rouabhia M. The Effects of Mentha x piperita Essential Oil on C. albicans Growth, Transition, Biofilm Formation, and the Expression of Secreted Aspartyl Proteinases Genes. Antibiotics. 2019;8:10. PubMed PMC
Van Den Dool H., Kratz P.D. A generalization of the retention index system including linear temperature programmed gas—Liquid partition chromatography. J. Chromatogr. A. 1963;11:463–471. doi: 10.1016/S0021-9673(01)80947-X. PubMed DOI