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Essential Oil Efficacy Impaired by Food Residues in Food Pathogen Adhesion

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Abstract

Bacterial adhesion is a complex process and influenced by the properties of the bacterial cell envelops and the surfaces to which bacteria are to attach. Most abiotic surfaces adsorb materials from the environment, and a conditioning layer will thus be formed that modifies the physicochemical properties of surface and the interaction with bacteria. After adhesion, bacteria can form biofilms, which pose a persistent threat in the food industry. Essential oils have the potential to inhibit adhesion and subsequently prevent biofilm formation. The aim of our study was to inhibit the adhesion of the food-borne pathogens of Bacillus cereus, Listeria monocytogenes, Staphylococcus aureus and methicillin resistant S. aureus (MRSA) onto native and with food residue-coated stainless steel (SS) and polypropylene (PP) surfaces by cinnamon, thyme and marjoram essential oils (EOs) by determining live cell count on the surfaces. Food residues on the SS and PP slides affected both the process of bacterial adhesion and the anti-adhesion action of investigated EOs: adhesion was supported, anti-adhesion effect was reduced. Thyme EO showed the best anti-adhesion effect: in sub-lethal concentration, it completely inhibited bacterial attachment of MRSA and L. monocytogenes to surfaces. Cinnamon EO always lost its anti-adhesion effect in the presence of food residues but was able to regain it after removing animal protein from the surface. In summary, it is essential to ensure proper cleaning before applying EO-based sanitization methods to enhance the effectiveness of the chosen essential oils.

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References

  1. Carpentier, B.; Cerf, O.: Persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 145, 1–8 (2011). https://doi.org/10.1016/j.ijfoodmicro.2011.01.005

    Article  Google Scholar 

  2. Bae, Y.M.; Baek, S.Y.; Lee, S.Y.: Resistance of pathogenic bacteria on the surface of stainless steel depending on attachment form and efficacy of chemical sanitizers. Int. J. Food Microbiol. 153, 465–473 (2012). https://doi.org/10.1016/j.ijfoodmicro.2011.12.017

    Article  Google Scholar 

  3. Giaouris, E.; Heir, E.; Hébraud, M.; Chorianopoulos, N.; Langsrud, S.; Møretrø, T.; Habimana, O.; Desvaux, M.; Renier, S.; Nychas, G.J.: Attachment and biofilm formation by foodborne bacteria in meat processing environments: Causes, implications, role of bacterial interactions and control by alternative novel methods. Meat Sci. 97(3), 298–309 (2014). https://doi.org/10.1016/j.meatsci.2013.05.023

    Article  Google Scholar 

  4. Goh, S.G.; Leile, A.H.; Kuan, C.H.; Loo, Y.Y.; Lye, Y.L.; Chang, W.S.; Soopna, P.; Najwa, M.S.; Tang, J.Y.H.; Yaya, R.; Nishibuchi, M.; Nakaguchi, Y.; Son, R.: Transmission of Listeria monocytogenes from raw chicken meat to cooked chicken meat through cutting boards. Food Control 37, 51–55 (2014). https://doi.org/10.1016/j.foodcont.2013.08.030

    Article  Google Scholar 

  5. Garrett, T.R.; Bhakoo, M.; Zhang, Z.: Bacterial adhesion and biofilms on surfaces. Prog. Nat. Sci. 18, 1049–1056 (2008). https://doi.org/10.1016/j.pnsc.2008.04.001

    Article  Google Scholar 

  6. Hori, K.; Matsumoto, S.: Bacterial adhesion: From mechanism to control. Biochem. Eng. J. 48, 424–434 (2010). https://doi.org/10.1016/j.bej.2009.11.014

    Article  Google Scholar 

  7. Busscher, H.J.; van der Mei, H.C.: How do bacteria know they are on a surface and regulate their response to an adhering state? PLoS Pathog. 8, e1002440 (2012). https://doi.org/10.1371/journal.ppat.1002440

    Article  Google Scholar 

  8. Petrova, O.E.; Sauer, K.: Sticky situations: Key components that control bacterial surface attachment. J. Bacteriol. 194, 2413–2425 (2012). https://doi.org/10.1128/JB.00003-12

    Article  Google Scholar 

  9. Srey, S.; Jahid, I.K.; Ha, S.D.: Biofilm formation in food industries: A food safety concern. Food Control 31, 572–585 (2013). https://doi.org/10.1016/j.foodcont.2012.12.001

    Article  Google Scholar 

  10. Tan, M.S.F.; White, A.P.; Rahman, S.; Dykes, G.A.: Role of fimbriae, flagella and cellulose on the attachment of Salmonella Typhimurium ATCC 14028 to plant cell wall models. PLoS ONE 11, e158311 (2016). https://doi.org/10.1371/journal.pone.0158311

    Article  Google Scholar 

  11. Cui, Y.; Walcott, R.; Chen, J.: Differential attachment of Salmonella enterica and enterohemorrhagic Escherichia coli to alfalfa, fenugreek, lettuce, and tomato seeds. Appl. Environ. Microbiol. (2017). https://doi.org/10.1128/AEM.03170-16

    Article  Google Scholar 

  12. Merget, B.; Forbes, K.J.; Brennan, F.; McAteer, S.; Shepherd, T.; Strachan, N.; Holden, N.J.: Influence of plant species, tissue type, and temperature on the capacity of Shiga-toxigenic Escherichia coli to colonize, grow, and be internalized by plants. Appl. Environ. Microbiol. 85, e00123-19 (2019). https://doi.org/10.1128/AEM.00123-19

    Article  Google Scholar 

  13. Mai, T.L.; Conner, D.E.: Effect of temperature and growth media on the attachment of Listeria monocytogenes to stainless steel. Int. J. Food Microbiol. 120, 282–286 (2007). https://doi.org/10.1016/j.ijfoodmicro.2007.09.006

    Article  Google Scholar 

  14. Dourou, D.; Beauchamp, C.S.; Yoon, Y.; Geornaras, I.; Belk, K.E.; Smith, G.C.; Nychas, G.E.; Sofos, J.N.: Attachment and biofilm formation by Escherichia coli O157:H7 at different temperatures, on various food-contact surfaces encountered in beef processing. Int. J. Food Microbiol. 149, 262–268 (2011). https://doi.org/10.1016/j.ijfoodmicro.2011.07.004

    Article  Google Scholar 

  15. Casarin, L.S.; Brandelli, A.; Casarin, F.O.; Soave, P.A.; Wanke, C.H.; Tondo, E.C.: Adhesion of Salmonella Enteritidis and Listeria monocytogenes on stainless steel welds. Int. J. Food Microbiol. 191, 103–108 (2014). https://doi.org/10.1016/j.ijfoodmicro.2014.09.003

    Article  Google Scholar 

  16. Yuan, L.; Hansen, M.F.; Roder, H.L.; Wang, N.; Burmolle, M.; He, G.: Mixed species biofilms in the food industry: current knowledge and novel control strategies. Crit. Rev. Food Sci. Nutr. 60, 2277–2293 (2020). https://doi.org/10.1080/10408398.2019.1632790

    Article  Google Scholar 

  17. Hermansson, M.: The DLVO theory in microbial adhesion. Col. Surf. B. Biointerf. 14, 105–119 (1999)

    Article  Google Scholar 

  18. Van Houdet, R.; Michiels, C.W.: Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res. Microbiol. 156, 626–633 (2006). https://doi.org/10.1016/j.resmic.2005.02.005

    Article  Google Scholar 

  19. Van Houdet, R.; Michiels, C.W.: Biofilm formation and the food industry, a focus on the bacteria outer surfaces. J. Appl. Microbiol. 109, 1117–1131 (2010). https://doi.org/10.1111/j.1365-2672.2010.04756.x

    Article  Google Scholar 

  20. Kyere, E.O.; Palmer, J.; Wargent, J.J.; Fletcher, G.C.; Flint, S.: Colonisation of lettuce by Listeria monocytogenes. Int. J. Food Sci. Technol. 54, 14–24 (2019). https://doi.org/10.1111/ijfs.13905

    Article  Google Scholar 

  21. Ruhal, R.; Kataria, R.: Biofilm patterns in gram-positive and gram-negative bacteria. Microbiol. Res. 251, 126829 (2021). https://doi.org/10.1016/j.micres.2021.126829

    Article  Google Scholar 

  22. Sangermani, M.; Hug, I.; Sauter, N.; Pfohl, T.; Jenal, U.: Tad pili play a dynamic role in Caulobacter crescentus surface colonization. MBio 10, 10–1128 (2019). https://doi.org/10.1128/mBio.01237-19

    Article  Google Scholar 

  23. Rossi, C.; Chaves-Lopez, C.; Mozzina, S.S.; Di Mattia, C.; Scuota, S.; Luzzi, I.; Jenic, T.; Paparella, A.; Serio, A.: Salmonella enterica adhesion: effect of Cinnamomum zeylanicum essential oil on lettuce. LWT Food Sci. Technol. 111, 16–22 (2019). https://doi.org/10.1016/j.lwt.2019.05.026

    Article  Google Scholar 

  24. Wang, C.; Hou, J.; van der Mei, H.C.; Busscher, H.J.; Ren, Y.: Emergent properties in Streptococcus mutans biofilms are controlled through adhesion force sensing by initial colonizers. MBio 10, e01908-19 (2019). https://doi.org/10.1128/mBio.01908-19

    Article  Google Scholar 

  25. Wang, L.; Fan, D.; Chen, W.; Terentjev, E.M.: Bacterial growth, detachment and cell size control on polyethylene terephthalate surfaces. Sci. Rep. 5, 15159 (2015). https://doi.org/10.1038/srep15159

    Article  Google Scholar 

  26. Alvarez-Ordóñez, A.L.; Coughlan, M.; Briandet, R.; Cotter, P.D.: Biofilms in food processing environments: challenges and opportunities. Annu. Rev. Food Sci. Technol. 10, 173–195 (2019). https://doi.org/10.1146/annurev-food-032818-121805

    Article  Google Scholar 

  27. Karampoula, F.; Doulgeraki, A.I.; Fotiadis, C.; Tampakaki, A.; Nychas, G.E.: Monitoring biofilm formation and microbial interactions that may occur during a Salmonella contamination incident across the network of a water bottling plant. Microorganisms. 7(8), 236 (2019). https://doi.org/10.3390/microorganisms7080236

    Article  Google Scholar 

  28. Carrascosa, C.; Raheem, D.; Ramos, F.; Saraiva, A.; Raposo, A.: Microbial biofilms in the food industry—a comprehensive review. Int. J. Environ. Res. Public Health 18(4), 2014 (2021). https://doi.org/10.3390/ijerph18042014

    Article  Google Scholar 

  29. Byun, K.H.; Han, S.H.; Yoon, J.; Park, S.H.; Ha, S.D.: Efficacy of chlorine based disinfectants (sodium hypochlorite and chlorine dioxide) on Salmonella Enteritidis planktonic cells, biofilms on food contact surfaces and chicken skin. Food Control 123, 107838 (2021). https://doi.org/10.1016/j.foodcont.2020.107838

    Article  Google Scholar 

  30. Mevo, S.I.U.; Ashrafudoulla, M.; Mizan, M.F.R.; Park, S.; Ha, S.D.: Promising strategies to control persistent enemies: some new technologies to combat biofilm in the food industry-a review. Comp. Rev. Food Sci. Food Safe. 20, 5938–5964 (2021). https://doi.org/10.1111/1541-4337.12852

    Article  Google Scholar 

  31. Szczepanski, S.; Lipski, A.: Essential oils show specific inhibiting effects on bacterial biofilm formation. Food Control 36, 224–229 (2014). https://doi.org/10.1016/j.foodcont.2013.08.023

    Article  Google Scholar 

  32. Shi, X.; Zhu, X.: Biofilm formation and food safety in food industries. Trends Food Sci. Tech. 20, 407–413 (2009). https://doi.org/10.1016/j.tifs.2009.01.054

    Article  Google Scholar 

  33. Bakkali, F.; Averbeck, S.; Averbeck, D.; Idaomar, M.: Biological effects of essential oils-A review. Food Chem. Toxicol. 46, 446–475 (2008). https://doi.org/10.1016/j.fct.2007.09.106

    Article  Google Scholar 

  34. Kerekes, E.B.; Vidács, A.; Takó, M.; Petkovits, T.; Vágvölgyi, C.; Horváth, G.; Balázs, V.L.; Krisch, J.: Anti-biofilm effect of selected essential oils and main components on mono- and polymicrobic bacterial cultures. Microorganisms. 7, 345 (2019). https://doi.org/10.3390/microorganisms7090345

    Article  Google Scholar 

  35. Kerekes, E.B.; Vidács, A.; Törökné, J. J.; Gömöri, Cs.; Takó, M.; Chandrasekaran, M.; Kadaikunnan, S.; Alharbi, N.S.; Krisch, J.; Vágvölgyi, Cs.: The Battle Against Microbial Pathogens: Basic Science, Technological Advances and Educational Programs. Essential oils against bacterial biofilm formation and quorum sensing of food-borne pathogens and spoilage microorganisms, vol. 1(5), pp. 429–437. Microbiology Book Series, Formatex Research Center, Badajoz (2015). ISBN 978-84-942134-6-5.

  36. Krisch, J.; Tserennadmid, R.; Vágvölgyi, C.: Interaction of essential oils and food components: consequences in food preservation. Essential oils as natural food additives. Composition, applications, antioxidant and antimicrobial properties. In: Valgimigli, L. (Ed.) Advances in Food Microbiology and Food Safety, pp. 361–377. Nova Science Publishers, Hauppauge, New York (2012)

    Google Scholar 

  37. Goulter, R.M.; Gentle, I.R.; Dykes, G.A.: Issues in determining factors influencing bacterial attachment: a review using the attachment of Escherichia coli to abiotic surfaces as an example. Let. Appl. Microbiol. 49, 1–7 (2009). https://doi.org/10.1111/j.1472-765X.2009.02591.x

    Article  Google Scholar 

  38. Prakash, B.; Veeregowda, B.M.; Krishnappa, G.: Biofilms: a survival strategy of bacteria. Curr. Sci. 85, 1299–1307 (2003)

    Google Scholar 

  39. Sarker, S.D.; Nahar, L.; Kumarasamy, Y.: Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 42, 321–324 (2007). https://doi.org/10.1016/j.ymeth.2007.01.006

    Article  Google Scholar 

  40. Jett, B.D.; Hatter, K.L.; Huycke, M.M.; Gilmore, M.S.: Simplified agar plate method for quantifying viable bacteria. Biotechniques 23, 648–650 (1997). https://doi.org/10.2144/97234bm22

    Article  Google Scholar 

  41. Hedge, J.E.; Hofreiter, B.T.: Methods in carbohydrate chemistry. In: Whistler, R.L.; BeMiller, J.N. (Eds.) Carbonhydrates, Vol. 17, p. 420. Academic Press, New York (1962)

    Google Scholar 

  42. Hungarian Standard MSZ 6380-11:1999 Animal feeding stuffs. Determination of nutritive value. Determination of peroxide number and acid number.

  43. da Silva, A.C.; Rodrigues, M.X.; Silva, N.C.C.: Methicillin-resistant Staphylococcus aureus in food and the prevalence in Brazil: a review. Braz. J. Microbiol. 51, 347–356 (2020). https://doi.org/10.1007/s42770-019-00168-1

    Article  Google Scholar 

  44. Lv, G.; Jiang, R.; Zhang, H.; Wang, L.; Li, L.; Gao, W.; Zhang, H.; Pei, Y.; Wei, X.; Dong, H.; Qin, L.: Molecular characteristics of Staphylococcus aureus from food samples and food poisoning outbreaks in Shijiazhuang, China. Front. Microbiol. 12, 652276 (2021). https://doi.org/10.3389/fmicb.2021.652276

    Article  Google Scholar 

  45. Nazzaro, F.; Fratianni, F.; De Martino, L.; Coppola, R.; de Feo, V.: Effect of essential oils on pathogenic bacteria. Pharmaceuticals. 6, 1451–1474 (2013). https://doi.org/10.3390/ph6121451

    Article  Google Scholar 

  46. An, Y.H.; Friedman, R.J.: Concise review of mechanism of bacterial adhesion to biomaterial surfaces. J. Biomed. Mater. Res. Part B Appl. Biomater. 43, 338–348 (1998). https://doi.org/10.1002/(sici)1097-4636(199823)43:3%3c338::aid-jbm16%3e3.0.co;2-b

    Article  Google Scholar 

  47. Debonne, E.; Van Bockstaele, F.; De Leyn, I.; Devlieghere, F.; Eeckhout, M.: Validation of in-vitro antifungal activity of thyme essential oil on Aspergillus niger and Penicillium paneum through application in parbaked wheat and sourdough bread. LWT Food Sci. Technol. 87, 368–378 (2018). https://doi.org/10.1016/j.lwt.2017.09.007

    Article  Google Scholar 

  48. Reyes-Jurado, F.; Navarro-Cruz, A.R.; Ochoa-Velasco, C.E.; Palou, E.; LópezMalo, A.; Ávila-Sosa, R.: Essential oils in vapor phase as alternative antimicrobials: a review. Crit. Rev. Food Sci. Nutr. 60, 1641–1650 (2020). https://doi.org/10.1080/10408398.2019.1586641

    Article  Google Scholar 

  49. Yu, L.; Shi, H.: Anti-adhesion mechanism of antimicrobial agents. Cur. O. Food Sci. 42, 8–14 (2021). https://doi.org/10.1016/j.cofs.2021.01.009

    Article  Google Scholar 

  50. Brown, H.L.; Reuter, M.; Salt, L.J.; Cross, K.L.; Betts, R.P.; van Vliet, A.H.M.: Chicken juice enhances surface attachment and biofilm formation of Campylobacter jejuni. Appl. Environ. Microbiol. 80, 7053–7060 (2014). https://doi.org/10.1128/AEM.02614-14

    Article  Google Scholar 

  51. Tomičić, Z.; Tomičić, R.; KocićTanackov, S.; Raspor, P.: Essential oils as antimicrobial and anti-adhesion agents against bacteria Salmonella Typhimurium and Staphylococcus aureus, and yeasts Candida albicans and Saccharomyces cerevisiae. Food Feed Res. 49(2), 107–115 (2022). https://doi.org/10.5937/ffr0-37683

    Article  Google Scholar 

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

    Google Scholar 

  53. Hyldgaard, M.; Mygind, T.; Meyer, R.L.: Essential oils in food preservation: mode of action, synergies, and interactions with food matrix components. Front. Microbiol. 3(12), 1–24 (2012). https://doi.org/10.3389/fmicb.2012.00012

    Article  Google Scholar 

  54. Vasconcelos, N.G.; Croda, J.; Simionatto, S.: Antibacterial mechanisms of cinnamon and its constituents: a review. Microb. Pathog. 120, 198–203 (2018). https://doi.org/10.1016/j.micpath.2018.04.036

    Article  Google Scholar 

  55. Bowker, B.C.; Zhuang, H.: Relationship between muscle exudate protein composition and broiler breast meat quality. Poultry Sci. 92, 1385–1392 (2013). https://doi.org/10.3382/ps.2012-02806

    Article  Google Scholar 

  56. Cáceres, M.; Hidalgo, W.; Stashenko, E.; Torres, R.; Ortiz, C.: Essential oils of aromatic plants with antibacterial, anti-biofilm and anti-quorum sensing activities against pathogenic bacteria. Antibiotics 9(4), 147 (2020). https://doi.org/10.3390/antibiotics9040147

    Article  Google Scholar 

  57. Müller, S.; Caron, N.G.: Functional single-cell analyses: flow cytometry and cell sorting of microbial populations and communities. FEMS Microbiol. Rev. 34(4), 554–587 (2010). https://doi.org/10.1111/j.1574-6976.2010.00214.x

    Article  Google Scholar 

  58. Ming, D.; Wang, D.; Cao, F.; **ang, H.; Mu, D.; Cao, J.; Li, B.; Zhong, L.; Dong, X.; Zhong, X.; Wang, L.; Wang, T.: Kaempferol inhibits the primary, attachment phase of biofilm formation in Staphylococcus aureus. Front. Microbiol. 8, 02263 (2017). https://doi.org/10.3389/fmicb.2017.02263

    Article  Google Scholar 

  59. Kuda, T.; Shibata, G.; Takahashi, H.; Kimura, B.: Effect of quantity of food residues on resistance to desiccation of food-related pathogens adhered to a stainless steel surface. Food Microbiol. 46, 234–238 (2015). https://doi.org/10.1016/j.fm.2014.08.014

    Article  Google Scholar 

  60. Vidács, A.; Kerekes, E.B.; Rajkó, R.; Petkovits, T.; Naiyf, S.A.; Jamal, M.K.; Vágvölgyi, C.; Krisch, J.: Optimization of essential oil-based natural disinfectants against Listeria monocytogenes and Escherichia coli biofilms formed on polypropylene surfaces. J. Mol. Liq. 255, 257–262 (2018). https://doi.org/10.1016/j.molliq.2018.01.179

    Article  Google Scholar 

  61. Amrutha, B.; Sundar, K.; Shetty, P.H.: Spice oil nanoemulsions: potential natural inhibitors against pathogenic E. coli and Salmonella spp. from fresh fruits and vegetables. LWT-Food Sci. Technol. 79, 152–159 (2017). https://doi.org/10.1016/j.lwt.2017.01.031

    Article  Google Scholar 

  62. Huang, K.; Nitin, N.: Antimicrobial particle-based novel sanitizer for enhanced decontamination of fresh produce. Appl. Environ. Microbiol. (2019). https://doi.org/10.1128/AEM.02599-18

    Article  Google Scholar 

  63. Cacciatore, A.F.; Dalmas, M.; Maders, C.; Isaıa, A.H.; Brandelli, A.; Malheiros, D.A.P.: Carvacrol encapsulation into, nanostructures: characterization and antimicrobial activity against foodborne pathogens adhered to stainless steel. Food Res. Int. 133, 109143 (2020). https://doi.org/10.1016/j.foodres.2020.109143

    Article  Google Scholar 

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Acknowledgements

This work was supported by the project GINOP-2.3.3-15-2016-00006 and GINOP 2.3.4-15-1234.

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Vidács, A., Bencsik-Kerekes, E.B., Ramteke, P.W. et al. Essential Oil Efficacy Impaired by Food Residues in Food Pathogen Adhesion. Arab J Sci Eng 49, 107–119 (2024). https://doi.org/10.1007/s13369-023-08415-2

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