Anticlostridial activity of the dill seed essential oil (Anetum graveolens L.): antibiofilm activity and antisporulation potential
Abstract
Clostridioides difficile is an anaerobic, spore-forming pathogen that causes serious toxin-mediated enteric disease in humans. In addition to antimicrobial resistance, biofilm and spore formation play key roles in the persistence of C. difficile in the gut, as well as in the transmission and relapse of the disease. In this study, the antimicrobial potential of dill seed essential oil on the planktonic growth of C. difficile clinical strains (isolated from stool specimens of hospitalized patients with diarrhea and confirmed Clostridioides difficile infection (CDI)) was investigated, along with its effect on biofilm and spore formation. The results showed varying degrees of antimicrobial activity, ranging from strong to weak, depending on the strain, with concentrations ranging from 0.08 to 40 mg/ml. The essential oil (EO) at concentrations of 2xMIC and MIC significantly reduced biofilm production in 89% and 84% of the tested strains, respectively. Spore formation was also significantly reduced when treated with 0.5xMIC and MIC of EO. Considering the anticlostridial activity of the dill seed EO, along with its inhibition of biofilm production and sporulation, this natural product is an excellent candidate for supplementary treatment of CDI.
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Aleksić, A., Stojanović-Radić, Z., Harmanus, C., Kuijper, E.J., & Stojanović, P. (2022). In vitro anti-clostridial action and potential of the spice herbs essential oils to prevent biofilm formation of hypervirulent Clostridioides difficile strains isolated from hospitalized patients with CDI. Anaerobe, 76, 102604. https://doi.org/10.1016/j.anaerobe.2022.102604
Aljarallah, K.M. (2016). Inhibition of Clostridium difficile by natural herbal extracts. Journal of Taibah University Medical Sciences, 11(5), 427–431. https://doi.org/10.1016/j.jtumed.2016.05.006
Awad, M.M., Johanesen, P.A., Carter, G.P., Rose, E., & Lyras, D. (2014). Clostridium difficile virulence factors: Insights into an anaerobic spore-forming pathogen. Gut Microbes, 5(5), 579–593. https://doi.org/10.4161/19490976.2014.969632
Babakhani, F., Bouillaut, L., Gomez, A., Sears, P., Nguyen, L., & Sonenshein, A.L. (2012). Fidaxomicin inhibits spore production in Clostridium difficile. Clinical Infectious Diseases, 55(SUPPL.2), 162–169. https://doi.org/10.1093/cid/cis453
Cermak, P., Olsovska, J., Mikyska, A., Dusek, M., Kadleckova, Z., Vanicek, J., Nyc, O., Sigler, K., Bostikova, V., & Bostik, P. (2017). Strong antimicrobial activity of xanthohumol and other derivatives from hops (Humulus lupulus L.) on gut anaerobic bacteria. APMIS, 1–6. https://doi.org/10.1111/apm.12747
Chahal, K., Monika, Kumar, A., Bhardwaj, U., & Kaur, R. (2017). Chemistry and biological activities of Anethum graveolens L. (dill) essential oil: A review. Journal of Pharmacognosy and Phytochemistry, 6(2), 295–306.
Chiu, C.W., Tsai, P.J., Lee, C.C., Ko, W.C., & Hung, Y.P. (2021). Inhibition of spores to prevent the recurrence of Clostridioides difficile infection - A possibility or an improbability? Journal of Microbiology, Immunology and Infection, 54(6), 1011–1017. https://doi.org/10.1016/j.jmii.2021.06.002
El-Tarabily, K. A., El-Saadony, M. T., Alagawany, M., Arif, M., Batiha, G.E., Khafaga, A.F., Elwan, H.A. M., Elnesr, S.S., & E. Abd El-Hack, M. (2021). Using essential oils to overcome bacterial biofilm formation and their antimicrobial resistance. Saudi Journal of Biological Sciences, 28(9), 5145–5156. https://doi.org/10.1016/j.sjbs.2021.05.033
Elgayyar, M., Draughon, F.A., Golden, D.A., & Mount, J.R. (2001). Antimicrobial activity of essential oils from plants against selected pathogenic and saprophytic microorganisms. Journal of Food Protection, 64(7), 1019–1024. https://doi.org/10.4315/0362-028X-64.7.1019
Figueroa, I., Johnson, S., Sambol, S.P., Goldstein, E.J.C., Citron, D.M., & Gerding, D.N. (2012). Relapse versus reinfection: Recurrent Clostridium difficile infection following treatment with fidaxomicin or vancomycin. Clinical Infectious Diseases, 55(SUPPL.2), 104–109. https://doi.org/10.1093/cid/cis357
Finegold, S.M., Summanen, P.H., Corbett, K., Downes, J., Henning, S., & Li, Z. (2014). Pomegranate Extract Exhibits in Vitro Activity Against Clostridium difficile. Nutrition. https://doi.org/10.1016/j.nut.2014.02.029
Frost, L.R., Cheng, J.K.J., & Unnikrishnan, M. (2021). Clostridioides difficile biofilms: A mechanism of persistence in the gut? PLoS Pathogens, 17(3), e1009348. https://doi.org/10.1371/journal.ppat.1009348
Garneau, J.R., Valiquette, L., & Fortier, L.C. (2014). Prevention of Clostridium difficile spore formation by sub-inhibitory concentrations of tigecycline and piperacillin/tazobactam. BMC Infectious Diseases, 14(29), 1–10. https://doi.org/10.1186/1471-2334-14-29
Harnvoravongchai, P., Chankhamhaengdecha, S., & Ounjai, P. (2018). Antimicrobial Effect of Asiatic Acid Against Clostridium difficile Is Associated With Disruption of Membrane Permeability. Frontiers in Microbiology, 9, 1–11. https://doi.org/10.3389/fmicb.2018.02125
Hussey, M., & Zayaits, A. (2016). Endospore Stain Protocol. In American Society for Microbiology (pp. 1–11).
Mishra, R., Panda, A.K., De Mandal, S., Shakeel, M., Bisht, S.S., & Khan, J. (2020). Natural Anti-biofilm Agents: Strategies to Control Biofilm-Forming Pathogens. Frontiers in Microbiology, 11(October). https://doi.org/10.3389/fmicb.2020.566325
Mooyottu, S., Flock, G., & Venkitanarayanan, K. (2017). Carvacrol reduces Clostridium difficile sporulation and spore outgrowth in vitro. Journal of Medical Microbiology, 66(8), 1229–1234. https://doi.org/10.1099/jmm.0.000515
Normington, C., Moura, I. B., Bryant, J.A., Ewin, D.J., Clark, E.V., Kettle, M.J., Harris, H.C., Spittal, W., Davis, G., Henn, M.R., Ford, C.B., Wilcox, M.H., & Buckley, A.M. (2021). Biofilms harbour Clostridioides difficile, serving as a reservoir for recurrent infection. Npj Biofilms and Microbiomes, 7(1). https://doi.org/10.1038/s41522-021-00184-w
Ozliman, S., Yaldiz, G., Camlica, M., & Ozsoy, N. (2021). Chemical components of essential oils and biological activities of the aqueous extract of Anethum graveolens L. grown under inorganic and organic conditions. Chemical and Biological Technologies in Agriculture, 8, 1–16. https://doi.org/10.1186/s40538-021-00224-9
Pejčić, M., Stojanović-Radić, Z., Dimitrijević, M., & Radulović, N. (2021). Antimicrobial efficacy of basil and sage essential oils against Pseudomonas aeruginosa: time-lapse kinetics and type of interaction with ciprofloxacin. Biologica Nyssana, 12(1), 47–54. https://doi.org/10.5281/zenodo.5522995
Petrof, E.O., Gloor, G.B., Vanner, S.J., Weese, S.J., Carter, D., Daigneault, M.C., Brown, E.M., Schroeter, K., & Allen-Vercoe, E. (2013). Stool substitute transplant therapy for the eradication of Clostridium difficile infection: “RePOOPulating” the gut. Microbiome, 1(1), 3. https://doi.org/10.1186/2049-2618-1-3
Phanchana, M., Harnvoravongchai, P., Wongkuna, S., Phetruen, T., Phothichaisri, W., Panturat, S., Pipatthana, M., Charoensutthivarakul, S., Chankhamhaengdecha, S., & Janvilisri, T. (2021). Frontiers in antibiotic alternatives for Clostridioides difficile infection. World Journal of Gastroenterology, 27(42), 7210–7232. https://doi.org/10.3748/wjg.v27.i42.7210
Poquet, I., Saujet, L., Canette, A., Monot, M., Mihajlovic, J., Ghigo, J. M., Soutourina, O., Briandet, R., Martin-Verstraete, I., & Dupuy, B. (2018). Clostridium difficile Biofilm: Remodeling metabolism and cell surface to build a sparse and heterogeneously aggregated architecture. Frontiers in Microbiology, 9, 1–20. https://doi.org/10.3389/fmicb.2018.02084
Roshan, N., Riley, T.V., & Hammer, K.A. (2017). Antimicrobial activity of natural products against Clostridium difficile in vitro. Journal of Applied Microbiology, 123, 92–103. https://doi.org/10.1111/jam.13486
Schäffler, H., & Breitrück, A. (2018). Clostridium difficile - From colonization to infection. Frontiers in Microbiology, 9, 1–12. https://doi.org/10.3389/fmicb.2018.00646
Schneider, C.A., Rasband, W.S., & Eliceiri, K.W. (2012). NIH Image to ImageJ: 25 years of Image Analysis HHS Public Access. Nature Methods, 9(7), 671–675.
Semenyuk, E.G., Laning, M.L., Foley, J., Johnston, P.F., Knight, K.L., Gerding, D.N., & Driks, A. (2014). Spore formation and toxin production in Clostridium difficile biofilms. PLoS ONE, 9(1). https://doi.org/10.1371/journal.pone.0087757
Sholeh, M., Krutova, M., Forouzesh, M., Mironov, S., Sadeghifard, N., Molaeipour, L., Maleki, A., & Kouhsari, E. (2020). Antimicrobial resistance in Clostridioides (Clostridium) difficile derived from humans: A systematic review and meta-analysis. Antimicrobial Resistance and Infection Control, 9(158), 1–11. https://doi.org/10.1186/s13756-020-00815-5
Stanojević, L. P., Stanković, M.Z., Cvetković, D.J., Danilović, B.R., & Stanojević, J.S. (2016). Dill (Anethum graveolens L.) seeds essential oil as a potential natural antioxidant and antimicrobial agent. Biologica Nyssana, 7(1), 31–39. https://doi.org/10.5281/zenodo.159101
Stepanović, S., Vuković, D., Hola, V., Di Bonaventura, G., Djukić, S., Ćircović, I., & Ruzicka, F. (2007). Quantification of biofilm in microtiter plates. APMIS, 115(8), 891–899.
Tijerina-Rodríguez, L., Villarreal-Treviño, L., Baines, S. D., Morfín-Otero, R., Camacho-Ortíz, A., Flores-Treviño, S., Maldonado-Garza, H., Rodríguez-Noriega, E., & Garza-González, E. (2019). High sporulation and overexpression of virulence factors in biofilms and reduced susceptibility to vancomycin and linezolid in recurrent Clostridium [Clostridioides] difficile infection isolates. PLoS ONE, 14(7), 1–14. https://doi.org/10.1371/journal.pone.0220671
Tortajada-Girbés, M., Rivas, A., Hernández, M., González, A., Ferrús, M. A., & Pina-Pérez, M.C. (2021). Alimentary and Pharmaceutical Approach to Natural Antimicrobials against Clostridioides difficile Gastrointestinal Infection. Foods, 10, 1124. https://doi.org/10.3390/foods10051124
Vuotto, C., Moura, I., Barbanti, F., Donelli, G., & Spigaglia, P. (2015). Sub-inhibitory concentrations of metronidazole increase biofilm formation in Clostridium difficile strains. Pathogens and Disease, 74(2), 1/26.
Vuotto, C., Moura, I., Barbanti, F., Donelli, G., & Spigaglia, P. (2016). Subinhibitory concentrations of metronidazole increase biofilm formation in Clostridium difficile strains. FEMS Pathogens and Disease, 74(July 2015), 1–7. https://doi.org/10.1093/femspd/ftv114
Wei, Y., Yang, F., Wu, Q., Gao, J., Liu, W., Liu, C., Guo, X., Suwal, S., Kou, Y., Zhang, B., Wang, Y., Zheng, K., & Tang, R. (2018). Protective effects of bifidobacterial strains against toxigenic Clostridium difficile. Frontiers in Microbiology, 9(MAY), 1–13. https://doi.org/10.3389/fmicb.2018.00888
Wultańska, D., Piotrowski, M., & Pituch, H. (2020). The effect of berberine chloride and/or its combination with vancomycin on the growth, biofilm formation, and motility of Clostridioides difficile. European Journal of Clinical Microbiology and Infectious Diseases, 39(7), 1391–1399. https://doi.org/10.1007/s10096-020-03857-0
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