Antibiofilm activity and mechanisms of Amomum tsao-ko and clove essential oils against Staphylococcus aureus
Main Article Content
Keywords
Staphylococcus aureus, biofilm, Amomum tsao-ko oil, clove oil
Abstract
Staphylococcus aureus biofilms significantly threaten public health by causing persistent infections and foodborne diseases. The rise in antibiotic resistance emphasizes the urgent need for effective non-antibiotic control strate-gies. This study evaluated the anti-biofilm potential of Amomum tsao-ko (AEO) and clove (CEO) essential oils against S. aureus NCTC8325. Gas chromatography–mass spectroscopy analysis revealed distinct chemical pro-files, with AEO exhibiting greater diversity. Both essential oils showed potent anti-biofilm activity against S. aureus NCTC8325, effectively preventing biofilm establishment, as confirmed by confocal laser scanning microscopy and scanning electron microscopy. The growth curves and crystal violet staining results demonstrated that AEO and CEO effectively inhibit biofilm formation at concentrations of 91.3 μg/mL and 86.3 μg/mL, respectively, without affecting bacterial growth. Transcriptomic profiling revealed that both AEO and CEO exert anti-biofilm effects through significant regulation of multiple molecular pathways. Interestingly, although the specific pathways influ-enced by AEO and CEO differed, both treatments significantly downregulated the S. aureus infection pathway and the expression of key adhesin protein genes within this pathway. Overall, this study provides critical insights into the phenotypic and transcriptional responses of S. aureus to AEO and CEO, thereby elucidating the molecu-lar basis of their anti-biofilm activities.
References
Alabdullatif, M. and Alzahrani, A. 2022. Expression of biofilm-associated genes in Staphylococcus aureus during storage of platelet concentrates. Transfusion and Apheresis Science 61(6): 103456. https://doi.org/10.1016/j.transci.2022.103456
Almeida, L., Lopes, N., Gaio, V., Cavaleiro, C., Salgueiro, L., Silva, V., Poeta, P. and Cerca, N. 2022. Thymbra capitata essential oil has a significant antimicrobial activity against methicillin-resistant Staphylococcus aureus pre-formed biofilms. Letters in Applied Microbiology 74(5): 787–795. https://doi.org/10.1111/lam.13665
Arciola, C.R., Campoccia, D. and Montanaro, L. 2018. Implant infections: adhesion, biofilm formation and immune evasion. Nature Reviews Microbiology 16(7): 397–409. https://doi.org/10.1038/s41579-018-0019-y
Aziz, Z. A. A., Ahmad, A., Setapar, S.H.M., Karakucuk, A., Azim, M.M., Lokhat, D., Rafatullah, M., Ganash, M., Kamal, M.A. and Ashraf, G.M. 2018. Essential oils: extraction techniques, pharmaceutical and therapeutic potential—a review. Current Drug Metabolism 19(13): 1100–1110. https://doi.org/10.2174/1389200219666180723144850
Böttcher, B., Driesch, D., Krüger, T., Garbe, E., Gerwien, F., Kniemeyer, O., Brakhage, A.A. and Vylkova, S. 2022. Impaired amino acid uptake leads to global metabolic imbalance of Candida albicans biofilms. NPJ Biofilms and Microbiomes 8: 78. https://doi.org/10.1038/s41522-022-00341-9
Cascioferro, S., Carbone, D., Parrino, B., Pecoraro, C., Giovannetti, E., Cirrincione, G. and Diana, P. 2021. Therapeutic strategies to counteract antibiotic resistance in MRSA biofilm-associated infections. ChemMedChem 16(1): 65–80. https://doi.org/10.1002/cmdc.202000677
Chen, J.W., Chen, J.L., Wang, Z.W., Chen, C.C., Zheng, J.X., Yu, Z.J., Deng, Q.W., Zhao, Y.X. and Wen, Z.W. 2022. 20S-ginsenoside Rg3 inhibits the biofilm formation and haemolytic activity of Staphylococcus aureus by inhibiting the SaeR/SaeS two-component system. Journal of Medical Microbiology 71(10): 001587 https://doi.org/10.1099/jmm.0.001587
Chen, L., Tang, Z.Y., Cui, S.Y., Ma, Z.B., Deng, H., Kong, W.L., Yang, L.W., Lin, C., Xiong, W.G. and Zeng, Z.L. 2020. Biofilm production ability, virulence and antimicrobial resistance genes in Staphylococcus aureus from various veterinary hospitals. Pathogens (Basel, Switzerland) 9(4): 264. https://doi.org/10.3390/pathogens9040264
Chung, D.R. and Huh, K. 2015. Novel pandemic influenza A (H1N1) and community-associated methicillin-resistant Staphylococcus aureus pneumonia. Expert Review of Anti-Infective Therapy 13(2): 197–207. https://doi.org/10.1586/14787210.2015.999668
Dai, M., Peng, C., Peng, F., Xie, C.B., Wang, P.J. and Sun, F.H. 2016a. Anti-Trichomonas vaginalis properties of the oil of Amomum tsao-ko and its major component, geraniol. Pharmaceutical Biology 54(3): 445–450. https://doi.org/10.3109/13880209.2015.1044617
Dai, M., Peng, C. and Sun, F.H. 2016b. Anti-infectious efficacy of essential oil from Caoguo (Fructus tsaoko). Journal of Traditional Chinese Medicine (Chung I Tsa Chih Ying Wen Pan) 36(6): 799–804. https://doi.org/10.1016/s0254-6272(17)30018-3
Dghais, S., Ben Jemaa, M., Chouchen, M., Jallouli, S., Ksouri, R. and Falleh, H. 2023. Nano-emulsification of cinnamon and curcuma essential oils for the quality improvement of minced meat beef. Foods (Basel, Switzerland) 12(2): 235. https://doi.org/10.3390/foods12020235
Elbestawy, M.K.M., El-Sherbiny, G.M. and Moghannem, S.A. 2023. Antibacterial, antibiofilm and anti-inflammatory activities of eugenol clove essential oil against resistant Helicobacter pylori. Molecules (Basel, Switzerland) 28(6): 2448. https://doi.org/10.3390/molecules28062448
Ersanli, C., Tzora, A., Skoufos, I., Fotou, K., Maloupa, E., Grigoriadou, K., Voidarou, C.C. and Zeugolis, D.I. 2023. The assessment of antimicrobial and anti-biofilm activity of essential oils against Staphylococcus aureus strains. Antibiotics (Basel, Switzerland) 12(2): 384. https://doi.org/10.3390/antibiotics12020384
Foster, C.E., Kok, M., Flores, A.R., Minard, C.G., Luna, R.A., Lamberth, L.B., Kaplan, S.L. and Hulten, K.G. 2020. Adhesin genes and biofilm formation among pediatric Staphylococcus aureus isolates from implant-associated infections. PloS One 15(6): e0235115. https://doi.org/10.1371/journal.pone.0235115
Gao, K.K., Su, B., Dai, J., Li, P., Wang, R.M. and Yang, X.H. 2022. Anti-biofilm and anti-hemolysis activities of 10-hydroxy-2-decenoic acid against Staphylococcus aureus. Molecules 27(5): 1485. https://doi.org/10.3390/molecules27051485
Guo, N., Bai, X., Shen, Y. and Zhang, T.H., 2023. Target-based screening for natural products against Staphylococcus aureus biofilms. Critical Reviews in Food Science and Nutrition 63(14): 2216–2230. https://doi.org/10.1080/10408398.2021.1972280
Hatlen, T.J. and Miller, L.G., 2021. Staphylococcal skin and soft tissue infections. Infectious Disease Clinics of North America 35(1): 81–105. https://doi.org/10.1016/j.idc.2020.10.003
He, Y.X., Yuan, Y., Gao, Y.Y., Chen, M.H., Li, Y.Y., Zou, Y., Liao, L.K., Li, X.T., Wang, Z., Li, J.H. and Zhou, W. 2024. Enhancement of colorimetric pH-sensitive film incorporating Amomum tsao-ko essential oil as antibacterial for mantis shrimp spoilage tracking and fresh-keeping. Foods (Basel, Switzerland) 13(11): 1638. https://doi.org/10.3390/foods13111638
Hernández-Cuellar, E., Tsuchiya, K., Valle-Ríos, R. and Medina-Contreras, O. 2023. Differences in biofilm formation by methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains. Diseases 11(4): 160. https://doi.org/10.3390/diseases11040160
Khatoon, Z., McTiernan, C.D., Suuronen, E.J., Mah, T.-F. and Alarcon, E.I. 2018. Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon 4(12): e01067. https://doi.org/10.1016/j.heliyon.2018.e01067
Kim, M.-S., Ahn, E.-K., Hong, S.S. and Oh, J.S. 2016. 2,8-Decadiene-1,10-diol inhibits lipopolysaccharide-induced inflammatory responses through inactivation of mitogen-activated protein kinase and nuclear factor-κB signaling pathway. Inflammation 39(2): 583–591. https://doi.org/10.1007/s10753-015-0283-1
Kim, D., Paggi, J.M., Park, C., Bennett, C. and Salzberg, S.L. 2019. Graph-based genome alignment and genotyping with HISAT2 and HISAT genotype. Nature Biotechnology 37(8): 907–915. https://doi.org/10.1038/s41587-019-0201-4
Klinger-Strobel, M., Stein, C., Forstner, C., Makarewicz, O. and Pletz, M.W., 2017. Effects of colistin on biofilm matrices of Escherichia coli and Staphylococcus aureus. International Journal of Antimicrobial Agents 49(4): 472–479. https://doi.org/10.1016/j.ijantimicag.2017.01.005
Lee, S.Y., Shetye, G.S., Son, S.-R., Lee, H., Klein, L.L., Yoshihara, J.K., Ma, R., Franzblau, S.G., Cho, S. and Jang, D.S. 2022. Anti-microbial activity of aliphatic alcohols from Chinese black cardamom (Amomum tsao-ko) against Mycobacterium tuberculosis H37Rv. Plants (Basel, Switzerland) 12(1): 34. https://doi.org/10.1016/j.ijantimicag.2017.01.005
Li, H., Li, J., Hua, Z.C., Aziz, T., Khojah, E., Cui, H.Y. and Lin, L. 2025. Transcriptomic combined with molecular dynamics simulation analysis of the inhibitory mechanism of clove essential oil against Staphylococcus aureus biofilm and its application on surface of food contact materials. Food and Bioproducts Processing 150: 131–140. https://doi.org/10.1016/j.fbp.2025.01.009
Li, W.D., Li, J.J., Qin, Z., Wang, Y., Zhao, P.Y. and Gao, H.Y. 2022a. Insights into the composition and antibacterial activity of Amomum tsao-ko essential oils from different regions based on GC-MS and GC-IMS. Foods 11(10): 1402. https://doi.org/10.3390/foods11101402
Li, J., Li, C., Shi, C., Aliakbarlu, J., Cui, H. and Lin, L. 2022b. Antibacterial mechanisms of clove essential oil against Staphylococcus aureus and its application in pork. International Journal of Food Microbiology 380: 109864. https://doi.org/10.1016/j.ijfoodmicro.2022.109864
Liñán-Atero, R., Aghababaei, F., García, S.R., Hasiri, Z., Ziogkas, D., Moreno, A. and Hadidi, M. 2024. Clove essential oil: chemical profile, biological activities, encapsulation strategies, and food applications. Antioxidants (Basel, Switzerland) 13(4): 488. https://doi.org/10.3390/antiox13040488
Liu, M., Wu, X., Li, J., Liu, L., Zhang, R., Shao, D. and Du, X. 2017. The specific anti-biofilm effect of gallic acid on Staphylococcus aureus by regulating the expression of the ica operon. Food Control 73: 613–618. https://doi.org/10.1016/j.foodcont.2016.09.015
Qian, W., Liu, M., Fu, Y., Zhang, J., Liu, W., Li, J., Li, X., Li, Y., and Wang, T. 2020. Antimicrobial mechanism of luteolin against Staphylococcus aureus and Listeria monocytogenes and its antibiofilm properties. Microbial pathogenesis, 142, 104056. https://doi.org/10.1016/j.micpath.2020.104056
Mahdi, A.A., Al-Maqtari, Q.A., Al-Ansi, W., Hu, W., Hashim, S.B.H., Cui, H.Y. and Lin, L. 2023. Replacement of polyethylene oxide by peach gum to produce an active film using Litsea cubeba essential oil and its application in beef. International Journal of Biological Macromolecules 241: 124592. https://doi.org/10.1016/j.ijbiomac.2023.124592
Mahmoudi, H., Pourhajibagher, M., Chiniforush, N., Soltanian, A.R., Alikhani, M.Y. and Bahador, A. 2019. Biofilm formation and antibiotic resistance in meticillin-resistant and meticillin-sensitive Staphylococcus aureus isolated from burns. Journal of Wound Care 28(2): 66–73. https://doi.org/10.12968/jowc.2019.28.2.66
Mamdoh, H., Hassanein, K.M., Eltoony, L.F., Khalifa, W.A., Hamed, E., Alshammari, T.O., Abd El-Kareem, D.M. and El-Mokhtar, M.A. 2023. Clinical and bacteriological analyses of biofilm-forming Staphylococci-isolated from diabetic foot ulcers. Infection and Drug Resistance 16: 1737–1750. https://doi.org/10.2147/IDR.S393724
Melander, R.J., Basak, A.K. and Melander, C. 2020. Natural products as inspiration for the development of bacterial antibiofilm agents. Natural Product Reports 37(11): 1454–1477. https://doi.org/10.1039/d0np00022a
Mitra, S., Thawrani, D., Banerjee, P., Gachhui, R. and Mukherjee, J. 2012. Induced biofilm cultivation enhances riboflavin production by an intertidally derived Candida famata. Applied Biochemistry and Biotechnology 166(8): 1991–2006. https://doi.org/10.1007/s12010-012-9626-7
Mohammadi Pelarti, S., Karimi Zarehshuran, L., Babaeekhou, L. and Ghane, M. 2021. Antibacterial, anti-biofilm and anti-quorum sensing activities of Artemisia dracunculus essential oil (EO): a study against Salmonella enterica serovar Typhimurium and Staphylococcus aureus. Archives of Microbiology 203(4): 1529–1537. https://doi.org/10.1007/s00203-020-02138-w
Neagu, R., Popovici, V., Ionescu, L.E., Ordeanu, V., Popescu, D.M., Ozon, E.A. and Gîrd, C.E. 2023. Antibacterial and antibiofilm effects of different samples of five commercially available essential oils. Antibiotics (Basel, Switzerland) 12(7): 1191. https://doi.org/10.3390/antibiotics12071191
Pant, N., Miranda-Hernandez, S., Rush, C., Warner, J. and Eisen, D.P. 2022. Non-antimicrobial adjuvant therapy using ticagrelor reduced biofilm-related Staphylococcus aureus prosthetic joint infection. Frontiers in Pharmacology 13: 927783. https://doi.org/10.3389/fphar.2022.927783
Pedonese, F., Longo, E., Torracca, B., Najar, B., Fratini, F. and Nuvoloni, R. 2022. Antimicrobial and anti-biofilm activity of manuka essential oil against Listeria monocytogenes and Staphylococcus aureus of food origin. Italian Journal of Food Safety 11(1): 10039. https://doi.org/10.4081/ijfs.2022.10039
Piechota, M., Kot, B., Frankowska-Maciejewska, A., Grużewska, A. and Woźniak-Kosek, A. 2018. Biofilm formation by methicillin-resistant and methicillin-sensitive Staphylococcus aureus strains from hospitalized patients in Poland. BioMed Research International 2018: 4657396. https://doi.org/10.1155/2018/4657396
Pires, D.P., Meneses, L., Brandão, A.C. and Azeredo, J. 2022. An overview of the current state of phage therapy for the treatment of biofilm-related infections. Current Opinion in Virology 53: 101209. https://doi.org/10.1016/j.coviro.2022.101209
Qiu, M., Long, N.N., Gao, M.X., Zhou, Y.Y., Sun, F.H., Lin, L. and Dai, M. 2019. In vitro anti-MRSA effect of clove oil combined with β-lactam antibiotics against methicillin-resistant Staphylococcus aureus. Chinese Herbal Medicines 50(7): 1629–1635. https://doi.org/10.7501/j.issn.0253-2670.2019.07.020
Quinn, T.P., Crowley, T.M. and Richardson, M.F. 2018. Benchmarking differential expression analysis tools for RNA-Seq: normalization-based vs. log-ratio transformation-based methods. BMC Bioinformatics 19(1): 274. https://doi.org/10.1186/s12859-018-2261-8
Rahimi, F., Katouli, M. and Karimi, S. 2016. Biofilm production among methicillin resistant Staphylococcus aureus strains isolated from catheterized patients with urinary tract infection. Microbial Pathogenesis 98: 69–76. https://doi.org/10.1016/j.micpath.2016.06.031
Rahman, M.R.T., Lou, Z., Yu, F., Wang, P. and Wang, H. 2017. Anti-quorum sensing and anti-biofilm activity of Amomum tsaoko (Amommum tsao-ko Crevost et Lemarie) on foodborne pathogens. Saudi Journal of Biological Sciences 24(2): 324–330. https://doi.org/10.1016/j.sjbs.2015.09.034
Rather, M.A., Gupta, K. and Mandal, M. 2021. Microbial biofilm: formation, architecture, antibiotic resistance, and control strategies. Brazilian Journal of Microbiology 52(4): 1701–1718. https://doi.org/10.1007/s42770-021-00624-x
Reis, S.V.D., Couto, N.M. G. de, Brust, F.R., Trentin, D.S., Silva, J.K.R. da, Arruda, M.S.P., Gnoatto, S.C.B. and Macedo, A.J. 2020. Remarkable capacity of Brosimine B to disrupt methicillin-resistant Staphylococcus aureus (MRSA) preformed biofilms. Microbial Pathogenesis 140: 103967. https://doi.org/10.1016/j.micpath.2020.103967
Ridyard, K.E. and Overhage, J. 2021. The potential of human peptide LL-37 as an antimicrobial and anti-biofilm agent. Antibiotics (Basel, Switzerland) 10(6): 650. https://doi.org/10.3390/antibiotics10060650
Roman, A.Y., Devred, F., Lobatchov, V.M., Makarov, A.A., Peyrot, V., Kubatiev, A.A. and Tsvetkov, P.O. 2016. Sequential binding of calcium ions to the B-repeat domain of SdrD from Staphylococcus aureus. Canadian Journal of Microbiology 62(2): 123–129. https://doi.org/10.1139/cjm-2015-0580
Silva, V., Almeida, L., Gaio, V., Cerca, N., Manageiro, V., Caniça, M., Capelo, J.L., Igrejas, G. and Poeta, P. 2021. Biofilm formation of multidrug-resistant MRSA strains isolated from different types of human infections. Pathogens (Basel, Switzerland) 10(8): 970. https://doi.org/10.3390/pathogens10080970
Somrani, M., Debbabi, H. and Palop, A. 2022. Antibacterial and antibiofilm activity of essential oil of clove against Listeria monocytogenes and Salmonella enteritidis. Food Science and Technology International (Ciencia Y Tecnologia De Los Alimentos Internacional) 28(4): 331–339. https://doi.org/10.1177/10820132211013273
Sultan, A.R., Swierstra, J.W., Lemmens-den Toom, N.A., Snijders, S.V., Hansenová Maňásková, S., Verbon, A. and van Wamel, W.J.B. 2018. Production of staphylococcal complement inhibitor (SCIN) and other immune modulators during the early stages of Staphylococcus aureus biofilm formation in a mammalian cell culture medium. Infection and Immunity 86(8): e00352-18. https://doi.org/10.1128/IAI.00352-18
Swearingen, M.C., Granger, J.F., Sullivan, A. and Stoodley, P. 2016. Elution of antibiotics from poly (methyl methacrylate) bone cement after extended implantation does not necessarily clear the infection despite susceptibility of the clinical isolates. Pathogens and Disease 74(1): ftv103. https://doi.org/10.1093/femspd/ftv103
Tong, S.Y.C., Davis, J.S., Eichenberger, E., Holland, T.L. and Fowler, V.G. 2015. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clinical Microbiology Reviews 28(3): 603–661. https://doi.org/10.1128/CMR.00134-14
Valarezo, E., Ledesma-Monteros, G., Jaramillo-Fierro, X., Radice, M. and Meneses, M.A. 2025. Antioxidant application of clove (Syzygium aromaticum) essential oil in meat and meat products: a systematic review. Plants 14(13): 1958. https://doi.org/10.3390/plants14131958
Vasile, C., Sivertsvik, M., Miteluţ, A.C., Brebu, M.A., Stoleru, E., Rosnes, J.T., Tănase, E.E., Khan, W., Pamfil, D., Cornea, C.P., Irimia, A. and Popa, M.E. 2017. Comparative analysis of the composition and active property evaluation of certain essential oils to assess their potential applications in active food packaging. Materials 10(1): 45. https://doi.org/10.3390/ma10010045
Vergara, A., Normanno, G., Di Ciccio, P., Pedonese, F., Nuvoloni, R., Parisi, A., Santagada, G., Colagiorgi, A., Zanardi, E., Ghidini, S. and Ianieri, A. 2017. Biofilm formation and its relationship with the molecular characteristics of food-related methicillin-resistant Staphylococcus aureus (MRSA). Journal of Food Science 82(10): 2364–2370. https://doi.org/10.1111/1750-3841.13846
Xie, L.B., Yu, D., Li, Y.N., Ju, H.D., Chen, J., Hu, L.X. and Yu, L.Q. 2022. Characterization, hypoglycemic activity, and antioxidant activity of methanol extracts from Amomum tsao-ko: in vitro and in vivo studies. Frontiers in Nutrition 9: 869749. https://doi.org/10.3389/fnut.2022.869749
Yan, Z.F., Guo, J.R., Chen, Q.M., Wan, S.B., Qin, Z. and Gao, H.Y. 2025. Antibiofilm activity of Amomum tsaoko essential oil on Staphylococcus aureus and its application in pork preservation. Foods (Basel, Switzerland) 14(4): 662. https://doi.org/10.3390/foods14040662
Yanakiev, S. 2020. Effects of cinnamon (Cinnamomum spp.) in dentistry: a review. Molecules (Basel, Switzerland) 25(18): 4184. https://doi.org/10.3390/molecules25184184
Yin, W., Wang, Y.T., Liu, L. and He, J. 2019. Biofilms: the microbial "protective clothing" in extreme environments. International Journal of Molecular Sciences 20(14): 3423. https://doi.org/10.3390/ijms20143423
Yu, J.Y., Han, W.H., Xu, Y.L., Shen, L., Zhao, H.L., Zhang, J., Xiao, Y.H., Guo, Y.J. and Yu, F.Y. 2024a. Biofilm-producing ability of methicillin-resistant Staphylococcus aureus clinically isolated in China. BMC Microbiology 24: 241. https://doi.org/10.1186/s12866-024-03380-8
Yu, X.H., Hu, E.H., Liu, F.Y., Zhang, Y., Li, W.W., Lyu, Y.M., Li, F.W., Wang, D.J. and Jin, W.B. 2024b. Preparation and characterization of polyphenol-chitosan conjugate-eugenol essential oil microcapsule and its effect on storage behavior of cherry tomato. Journal of Food Science 89(12): 9577–9594. https://doi.org/10.1111/1750-3841.17524
Zhang, T.-T., Lu, C.-L. and Jiang, J.-G. 2015. Antioxidant and anti-tumour evaluation of compounds identified from fruit of Amomum tsaoko Crevost et Lemaire. Journal of Functional Foods 18: 423–431. https://doi.org/10.1016/j.jff.2015.08.005
Almeida, L., Lopes, N., Gaio, V., Cavaleiro, C., Salgueiro, L., Silva, V., Poeta, P. and Cerca, N. 2022. Thymbra capitata essential oil has a significant antimicrobial activity against methicillin-resistant Staphylococcus aureus pre-formed biofilms. Letters in Applied Microbiology 74(5): 787–795. https://doi.org/10.1111/lam.13665
Arciola, C.R., Campoccia, D. and Montanaro, L. 2018. Implant infections: adhesion, biofilm formation and immune evasion. Nature Reviews Microbiology 16(7): 397–409. https://doi.org/10.1038/s41579-018-0019-y
Aziz, Z. A. A., Ahmad, A., Setapar, S.H.M., Karakucuk, A., Azim, M.M., Lokhat, D., Rafatullah, M., Ganash, M., Kamal, M.A. and Ashraf, G.M. 2018. Essential oils: extraction techniques, pharmaceutical and therapeutic potential—a review. Current Drug Metabolism 19(13): 1100–1110. https://doi.org/10.2174/1389200219666180723144850
Böttcher, B., Driesch, D., Krüger, T., Garbe, E., Gerwien, F., Kniemeyer, O., Brakhage, A.A. and Vylkova, S. 2022. Impaired amino acid uptake leads to global metabolic imbalance of Candida albicans biofilms. NPJ Biofilms and Microbiomes 8: 78. https://doi.org/10.1038/s41522-022-00341-9
Cascioferro, S., Carbone, D., Parrino, B., Pecoraro, C., Giovannetti, E., Cirrincione, G. and Diana, P. 2021. Therapeutic strategies to counteract antibiotic resistance in MRSA biofilm-associated infections. ChemMedChem 16(1): 65–80. https://doi.org/10.1002/cmdc.202000677
Chen, J.W., Chen, J.L., Wang, Z.W., Chen, C.C., Zheng, J.X., Yu, Z.J., Deng, Q.W., Zhao, Y.X. and Wen, Z.W. 2022. 20S-ginsenoside Rg3 inhibits the biofilm formation and haemolytic activity of Staphylococcus aureus by inhibiting the SaeR/SaeS two-component system. Journal of Medical Microbiology 71(10): 001587 https://doi.org/10.1099/jmm.0.001587
Chen, L., Tang, Z.Y., Cui, S.Y., Ma, Z.B., Deng, H., Kong, W.L., Yang, L.W., Lin, C., Xiong, W.G. and Zeng, Z.L. 2020. Biofilm production ability, virulence and antimicrobial resistance genes in Staphylococcus aureus from various veterinary hospitals. Pathogens (Basel, Switzerland) 9(4): 264. https://doi.org/10.3390/pathogens9040264
Chung, D.R. and Huh, K. 2015. Novel pandemic influenza A (H1N1) and community-associated methicillin-resistant Staphylococcus aureus pneumonia. Expert Review of Anti-Infective Therapy 13(2): 197–207. https://doi.org/10.1586/14787210.2015.999668
Dai, M., Peng, C., Peng, F., Xie, C.B., Wang, P.J. and Sun, F.H. 2016a. Anti-Trichomonas vaginalis properties of the oil of Amomum tsao-ko and its major component, geraniol. Pharmaceutical Biology 54(3): 445–450. https://doi.org/10.3109/13880209.2015.1044617
Dai, M., Peng, C. and Sun, F.H. 2016b. Anti-infectious efficacy of essential oil from Caoguo (Fructus tsaoko). Journal of Traditional Chinese Medicine (Chung I Tsa Chih Ying Wen Pan) 36(6): 799–804. https://doi.org/10.1016/s0254-6272(17)30018-3
Dghais, S., Ben Jemaa, M., Chouchen, M., Jallouli, S., Ksouri, R. and Falleh, H. 2023. Nano-emulsification of cinnamon and curcuma essential oils for the quality improvement of minced meat beef. Foods (Basel, Switzerland) 12(2): 235. https://doi.org/10.3390/foods12020235
Elbestawy, M.K.M., El-Sherbiny, G.M. and Moghannem, S.A. 2023. Antibacterial, antibiofilm and anti-inflammatory activities of eugenol clove essential oil against resistant Helicobacter pylori. Molecules (Basel, Switzerland) 28(6): 2448. https://doi.org/10.3390/molecules28062448
Ersanli, C., Tzora, A., Skoufos, I., Fotou, K., Maloupa, E., Grigoriadou, K., Voidarou, C.C. and Zeugolis, D.I. 2023. The assessment of antimicrobial and anti-biofilm activity of essential oils against Staphylococcus aureus strains. Antibiotics (Basel, Switzerland) 12(2): 384. https://doi.org/10.3390/antibiotics12020384
Foster, C.E., Kok, M., Flores, A.R., Minard, C.G., Luna, R.A., Lamberth, L.B., Kaplan, S.L. and Hulten, K.G. 2020. Adhesin genes and biofilm formation among pediatric Staphylococcus aureus isolates from implant-associated infections. PloS One 15(6): e0235115. https://doi.org/10.1371/journal.pone.0235115
Gao, K.K., Su, B., Dai, J., Li, P., Wang, R.M. and Yang, X.H. 2022. Anti-biofilm and anti-hemolysis activities of 10-hydroxy-2-decenoic acid against Staphylococcus aureus. Molecules 27(5): 1485. https://doi.org/10.3390/molecules27051485
Guo, N., Bai, X., Shen, Y. and Zhang, T.H., 2023. Target-based screening for natural products against Staphylococcus aureus biofilms. Critical Reviews in Food Science and Nutrition 63(14): 2216–2230. https://doi.org/10.1080/10408398.2021.1972280
Hatlen, T.J. and Miller, L.G., 2021. Staphylococcal skin and soft tissue infections. Infectious Disease Clinics of North America 35(1): 81–105. https://doi.org/10.1016/j.idc.2020.10.003
He, Y.X., Yuan, Y., Gao, Y.Y., Chen, M.H., Li, Y.Y., Zou, Y., Liao, L.K., Li, X.T., Wang, Z., Li, J.H. and Zhou, W. 2024. Enhancement of colorimetric pH-sensitive film incorporating Amomum tsao-ko essential oil as antibacterial for mantis shrimp spoilage tracking and fresh-keeping. Foods (Basel, Switzerland) 13(11): 1638. https://doi.org/10.3390/foods13111638
Hernández-Cuellar, E., Tsuchiya, K., Valle-Ríos, R. and Medina-Contreras, O. 2023. Differences in biofilm formation by methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains. Diseases 11(4): 160. https://doi.org/10.3390/diseases11040160
Khatoon, Z., McTiernan, C.D., Suuronen, E.J., Mah, T.-F. and Alarcon, E.I. 2018. Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon 4(12): e01067. https://doi.org/10.1016/j.heliyon.2018.e01067
Kim, M.-S., Ahn, E.-K., Hong, S.S. and Oh, J.S. 2016. 2,8-Decadiene-1,10-diol inhibits lipopolysaccharide-induced inflammatory responses through inactivation of mitogen-activated protein kinase and nuclear factor-κB signaling pathway. Inflammation 39(2): 583–591. https://doi.org/10.1007/s10753-015-0283-1
Kim, D., Paggi, J.M., Park, C., Bennett, C. and Salzberg, S.L. 2019. Graph-based genome alignment and genotyping with HISAT2 and HISAT genotype. Nature Biotechnology 37(8): 907–915. https://doi.org/10.1038/s41587-019-0201-4
Klinger-Strobel, M., Stein, C., Forstner, C., Makarewicz, O. and Pletz, M.W., 2017. Effects of colistin on biofilm matrices of Escherichia coli and Staphylococcus aureus. International Journal of Antimicrobial Agents 49(4): 472–479. https://doi.org/10.1016/j.ijantimicag.2017.01.005
Lee, S.Y., Shetye, G.S., Son, S.-R., Lee, H., Klein, L.L., Yoshihara, J.K., Ma, R., Franzblau, S.G., Cho, S. and Jang, D.S. 2022. Anti-microbial activity of aliphatic alcohols from Chinese black cardamom (Amomum tsao-ko) against Mycobacterium tuberculosis H37Rv. Plants (Basel, Switzerland) 12(1): 34. https://doi.org/10.1016/j.ijantimicag.2017.01.005
Li, H., Li, J., Hua, Z.C., Aziz, T., Khojah, E., Cui, H.Y. and Lin, L. 2025. Transcriptomic combined with molecular dynamics simulation analysis of the inhibitory mechanism of clove essential oil against Staphylococcus aureus biofilm and its application on surface of food contact materials. Food and Bioproducts Processing 150: 131–140. https://doi.org/10.1016/j.fbp.2025.01.009
Li, W.D., Li, J.J., Qin, Z., Wang, Y., Zhao, P.Y. and Gao, H.Y. 2022a. Insights into the composition and antibacterial activity of Amomum tsao-ko essential oils from different regions based on GC-MS and GC-IMS. Foods 11(10): 1402. https://doi.org/10.3390/foods11101402
Li, J., Li, C., Shi, C., Aliakbarlu, J., Cui, H. and Lin, L. 2022b. Antibacterial mechanisms of clove essential oil against Staphylococcus aureus and its application in pork. International Journal of Food Microbiology 380: 109864. https://doi.org/10.1016/j.ijfoodmicro.2022.109864
Liñán-Atero, R., Aghababaei, F., García, S.R., Hasiri, Z., Ziogkas, D., Moreno, A. and Hadidi, M. 2024. Clove essential oil: chemical profile, biological activities, encapsulation strategies, and food applications. Antioxidants (Basel, Switzerland) 13(4): 488. https://doi.org/10.3390/antiox13040488
Liu, M., Wu, X., Li, J., Liu, L., Zhang, R., Shao, D. and Du, X. 2017. The specific anti-biofilm effect of gallic acid on Staphylococcus aureus by regulating the expression of the ica operon. Food Control 73: 613–618. https://doi.org/10.1016/j.foodcont.2016.09.015
Qian, W., Liu, M., Fu, Y., Zhang, J., Liu, W., Li, J., Li, X., Li, Y., and Wang, T. 2020. Antimicrobial mechanism of luteolin against Staphylococcus aureus and Listeria monocytogenes and its antibiofilm properties. Microbial pathogenesis, 142, 104056. https://doi.org/10.1016/j.micpath.2020.104056
Mahdi, A.A., Al-Maqtari, Q.A., Al-Ansi, W., Hu, W., Hashim, S.B.H., Cui, H.Y. and Lin, L. 2023. Replacement of polyethylene oxide by peach gum to produce an active film using Litsea cubeba essential oil and its application in beef. International Journal of Biological Macromolecules 241: 124592. https://doi.org/10.1016/j.ijbiomac.2023.124592
Mahmoudi, H., Pourhajibagher, M., Chiniforush, N., Soltanian, A.R., Alikhani, M.Y. and Bahador, A. 2019. Biofilm formation and antibiotic resistance in meticillin-resistant and meticillin-sensitive Staphylococcus aureus isolated from burns. Journal of Wound Care 28(2): 66–73. https://doi.org/10.12968/jowc.2019.28.2.66
Mamdoh, H., Hassanein, K.M., Eltoony, L.F., Khalifa, W.A., Hamed, E., Alshammari, T.O., Abd El-Kareem, D.M. and El-Mokhtar, M.A. 2023. Clinical and bacteriological analyses of biofilm-forming Staphylococci-isolated from diabetic foot ulcers. Infection and Drug Resistance 16: 1737–1750. https://doi.org/10.2147/IDR.S393724
Melander, R.J., Basak, A.K. and Melander, C. 2020. Natural products as inspiration for the development of bacterial antibiofilm agents. Natural Product Reports 37(11): 1454–1477. https://doi.org/10.1039/d0np00022a
Mitra, S., Thawrani, D., Banerjee, P., Gachhui, R. and Mukherjee, J. 2012. Induced biofilm cultivation enhances riboflavin production by an intertidally derived Candida famata. Applied Biochemistry and Biotechnology 166(8): 1991–2006. https://doi.org/10.1007/s12010-012-9626-7
Mohammadi Pelarti, S., Karimi Zarehshuran, L., Babaeekhou, L. and Ghane, M. 2021. Antibacterial, anti-biofilm and anti-quorum sensing activities of Artemisia dracunculus essential oil (EO): a study against Salmonella enterica serovar Typhimurium and Staphylococcus aureus. Archives of Microbiology 203(4): 1529–1537. https://doi.org/10.1007/s00203-020-02138-w
Neagu, R., Popovici, V., Ionescu, L.E., Ordeanu, V., Popescu, D.M., Ozon, E.A. and Gîrd, C.E. 2023. Antibacterial and antibiofilm effects of different samples of five commercially available essential oils. Antibiotics (Basel, Switzerland) 12(7): 1191. https://doi.org/10.3390/antibiotics12071191
Pant, N., Miranda-Hernandez, S., Rush, C., Warner, J. and Eisen, D.P. 2022. Non-antimicrobial adjuvant therapy using ticagrelor reduced biofilm-related Staphylococcus aureus prosthetic joint infection. Frontiers in Pharmacology 13: 927783. https://doi.org/10.3389/fphar.2022.927783
Pedonese, F., Longo, E., Torracca, B., Najar, B., Fratini, F. and Nuvoloni, R. 2022. Antimicrobial and anti-biofilm activity of manuka essential oil against Listeria monocytogenes and Staphylococcus aureus of food origin. Italian Journal of Food Safety 11(1): 10039. https://doi.org/10.4081/ijfs.2022.10039
Piechota, M., Kot, B., Frankowska-Maciejewska, A., Grużewska, A. and Woźniak-Kosek, A. 2018. Biofilm formation by methicillin-resistant and methicillin-sensitive Staphylococcus aureus strains from hospitalized patients in Poland. BioMed Research International 2018: 4657396. https://doi.org/10.1155/2018/4657396
Pires, D.P., Meneses, L., Brandão, A.C. and Azeredo, J. 2022. An overview of the current state of phage therapy for the treatment of biofilm-related infections. Current Opinion in Virology 53: 101209. https://doi.org/10.1016/j.coviro.2022.101209
Qiu, M., Long, N.N., Gao, M.X., Zhou, Y.Y., Sun, F.H., Lin, L. and Dai, M. 2019. In vitro anti-MRSA effect of clove oil combined with β-lactam antibiotics against methicillin-resistant Staphylococcus aureus. Chinese Herbal Medicines 50(7): 1629–1635. https://doi.org/10.7501/j.issn.0253-2670.2019.07.020
Quinn, T.P., Crowley, T.M. and Richardson, M.F. 2018. Benchmarking differential expression analysis tools for RNA-Seq: normalization-based vs. log-ratio transformation-based methods. BMC Bioinformatics 19(1): 274. https://doi.org/10.1186/s12859-018-2261-8
Rahimi, F., Katouli, M. and Karimi, S. 2016. Biofilm production among methicillin resistant Staphylococcus aureus strains isolated from catheterized patients with urinary tract infection. Microbial Pathogenesis 98: 69–76. https://doi.org/10.1016/j.micpath.2016.06.031
Rahman, M.R.T., Lou, Z., Yu, F., Wang, P. and Wang, H. 2017. Anti-quorum sensing and anti-biofilm activity of Amomum tsaoko (Amommum tsao-ko Crevost et Lemarie) on foodborne pathogens. Saudi Journal of Biological Sciences 24(2): 324–330. https://doi.org/10.1016/j.sjbs.2015.09.034
Rather, M.A., Gupta, K. and Mandal, M. 2021. Microbial biofilm: formation, architecture, antibiotic resistance, and control strategies. Brazilian Journal of Microbiology 52(4): 1701–1718. https://doi.org/10.1007/s42770-021-00624-x
Reis, S.V.D., Couto, N.M. G. de, Brust, F.R., Trentin, D.S., Silva, J.K.R. da, Arruda, M.S.P., Gnoatto, S.C.B. and Macedo, A.J. 2020. Remarkable capacity of Brosimine B to disrupt methicillin-resistant Staphylococcus aureus (MRSA) preformed biofilms. Microbial Pathogenesis 140: 103967. https://doi.org/10.1016/j.micpath.2020.103967
Ridyard, K.E. and Overhage, J. 2021. The potential of human peptide LL-37 as an antimicrobial and anti-biofilm agent. Antibiotics (Basel, Switzerland) 10(6): 650. https://doi.org/10.3390/antibiotics10060650
Roman, A.Y., Devred, F., Lobatchov, V.M., Makarov, A.A., Peyrot, V., Kubatiev, A.A. and Tsvetkov, P.O. 2016. Sequential binding of calcium ions to the B-repeat domain of SdrD from Staphylococcus aureus. Canadian Journal of Microbiology 62(2): 123–129. https://doi.org/10.1139/cjm-2015-0580
Silva, V., Almeida, L., Gaio, V., Cerca, N., Manageiro, V., Caniça, M., Capelo, J.L., Igrejas, G. and Poeta, P. 2021. Biofilm formation of multidrug-resistant MRSA strains isolated from different types of human infections. Pathogens (Basel, Switzerland) 10(8): 970. https://doi.org/10.3390/pathogens10080970
Somrani, M., Debbabi, H. and Palop, A. 2022. Antibacterial and antibiofilm activity of essential oil of clove against Listeria monocytogenes and Salmonella enteritidis. Food Science and Technology International (Ciencia Y Tecnologia De Los Alimentos Internacional) 28(4): 331–339. https://doi.org/10.1177/10820132211013273
Sultan, A.R., Swierstra, J.W., Lemmens-den Toom, N.A., Snijders, S.V., Hansenová Maňásková, S., Verbon, A. and van Wamel, W.J.B. 2018. Production of staphylococcal complement inhibitor (SCIN) and other immune modulators during the early stages of Staphylococcus aureus biofilm formation in a mammalian cell culture medium. Infection and Immunity 86(8): e00352-18. https://doi.org/10.1128/IAI.00352-18
Swearingen, M.C., Granger, J.F., Sullivan, A. and Stoodley, P. 2016. Elution of antibiotics from poly (methyl methacrylate) bone cement after extended implantation does not necessarily clear the infection despite susceptibility of the clinical isolates. Pathogens and Disease 74(1): ftv103. https://doi.org/10.1093/femspd/ftv103
Tong, S.Y.C., Davis, J.S., Eichenberger, E., Holland, T.L. and Fowler, V.G. 2015. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clinical Microbiology Reviews 28(3): 603–661. https://doi.org/10.1128/CMR.00134-14
Valarezo, E., Ledesma-Monteros, G., Jaramillo-Fierro, X., Radice, M. and Meneses, M.A. 2025. Antioxidant application of clove (Syzygium aromaticum) essential oil in meat and meat products: a systematic review. Plants 14(13): 1958. https://doi.org/10.3390/plants14131958
Vasile, C., Sivertsvik, M., Miteluţ, A.C., Brebu, M.A., Stoleru, E., Rosnes, J.T., Tănase, E.E., Khan, W., Pamfil, D., Cornea, C.P., Irimia, A. and Popa, M.E. 2017. Comparative analysis of the composition and active property evaluation of certain essential oils to assess their potential applications in active food packaging. Materials 10(1): 45. https://doi.org/10.3390/ma10010045
Vergara, A., Normanno, G., Di Ciccio, P., Pedonese, F., Nuvoloni, R., Parisi, A., Santagada, G., Colagiorgi, A., Zanardi, E., Ghidini, S. and Ianieri, A. 2017. Biofilm formation and its relationship with the molecular characteristics of food-related methicillin-resistant Staphylococcus aureus (MRSA). Journal of Food Science 82(10): 2364–2370. https://doi.org/10.1111/1750-3841.13846
Xie, L.B., Yu, D., Li, Y.N., Ju, H.D., Chen, J., Hu, L.X. and Yu, L.Q. 2022. Characterization, hypoglycemic activity, and antioxidant activity of methanol extracts from Amomum tsao-ko: in vitro and in vivo studies. Frontiers in Nutrition 9: 869749. https://doi.org/10.3389/fnut.2022.869749
Yan, Z.F., Guo, J.R., Chen, Q.M., Wan, S.B., Qin, Z. and Gao, H.Y. 2025. Antibiofilm activity of Amomum tsaoko essential oil on Staphylococcus aureus and its application in pork preservation. Foods (Basel, Switzerland) 14(4): 662. https://doi.org/10.3390/foods14040662
Yanakiev, S. 2020. Effects of cinnamon (Cinnamomum spp.) in dentistry: a review. Molecules (Basel, Switzerland) 25(18): 4184. https://doi.org/10.3390/molecules25184184
Yin, W., Wang, Y.T., Liu, L. and He, J. 2019. Biofilms: the microbial "protective clothing" in extreme environments. International Journal of Molecular Sciences 20(14): 3423. https://doi.org/10.3390/ijms20143423
Yu, J.Y., Han, W.H., Xu, Y.L., Shen, L., Zhao, H.L., Zhang, J., Xiao, Y.H., Guo, Y.J. and Yu, F.Y. 2024a. Biofilm-producing ability of methicillin-resistant Staphylococcus aureus clinically isolated in China. BMC Microbiology 24: 241. https://doi.org/10.1186/s12866-024-03380-8
Yu, X.H., Hu, E.H., Liu, F.Y., Zhang, Y., Li, W.W., Lyu, Y.M., Li, F.W., Wang, D.J. and Jin, W.B. 2024b. Preparation and characterization of polyphenol-chitosan conjugate-eugenol essential oil microcapsule and its effect on storage behavior of cherry tomato. Journal of Food Science 89(12): 9577–9594. https://doi.org/10.1111/1750-3841.17524
Zhang, T.-T., Lu, C.-L. and Jiang, J.-G. 2015. Antioxidant and anti-tumour evaluation of compounds identified from fruit of Amomum tsaoko Crevost et Lemaire. Journal of Functional Foods 18: 423–431. https://doi.org/10.1016/j.jff.2015.08.005
Article Sidebar
Published
Mar 20, 2026
Article Details
Section
Original Article
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
