Disinfectant test against monoculture and mixed-culture biofilms composed of technological, spoilage and pathogenic bacteria: Bactericidal effect of essential oil and hydrosol of Satureja thymbra and comparison with standard acid-base sanitizers
Abstract
AIMS: To assess the antimicrobial action of three natural-derived products (essential oil, decoction and hydrosol of Satureja thymbra) against biofilms, composed of useful, spoilage and pathogenic bacteria (formed as monoculture or/and mixed-culture), and to compare their efficiency with three standard acid and alkaline chemical disinfectants. METHODS AND RESULTS: Two acids (hydrochloric and lactic, pH 3), one alkali (sodium hydroxide, pH 11), the essential oil of S. thymbra (1% v/v) and the two by-products of the essential oil purification procedure (the decoction and the hydrosol fraction of essential oil, 100%), were tested against biofilms formed by five bacterial species, either as monospecies, or as mixed-culture of all species. The tested bacterial species were Staphylococcus simulans and Lactobacillus fermentum (useful technological bacteria), Pseudomonas putida (spoilage bacterium), Salmonella enterica and Listeria monocytogenes (pathogenic bacteria). Biofilms were left to be formed on stainless steel coupons for 5 days at 16 degrees C, before the application of disinfection treatments, for 60 and 180 min. The disinfection efficiency was evaluated by detaching the remaining viable biofilm cells and enumerating them by agar plating, as well as by automated conductance measurements (using Rapid Automated Bacterial Impedance Technique). Both these methods revealed that the essential oil and the hydrosol of S. thymbra exhibited a strong antimicrobial action against both monospecies and mixed-culture biofilms. Surprisingly, the efficiency of the other three acid-base disinfectants was not adequate, although a long antimicrobial treatment was applied (180 min). CONCLUSIONS: The essential oil of S. thymbra (1%), as well as its hydrosol fraction (100%), presents sufficient bactericidal effect on bacterial biofilms formed on stainless steel. SIGNIFICANCE AND IMPACT OF THE STUDY: Use of natural antimicrobial agents could provide alternative or supplemented ways for the disinfection of microbial-contaminated industrial surfaces.
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Essential oils contain a wide variety of secondary metabolites capable of inhibiting or slowing the growth of bacteria, yeasts and moulds.
“EOs contain a wide series of secondary metabolites that can inhibit or slow the growth of bacteria, yeasts and moulds [3,4,5].”
From Effect of essential oils on pathogenic bacteria (2013) · cites this paper as [3]
Cites
Essential oils: Their antibacterial properties and potential applications in foods—A review
Burt, S. (2004) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2004.03.022 · Cited by 10,488 · see citing works
Mechanisms of biofilm resistance to antimicrobial agents
Mah, T.-F. C., & O'Toole, G. A. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01913-2 · Cited by 3,921 · see citing works
Food microbiology : fundamentals and frontiers
Doyle, M. P., Beuchat, L. R., & Montville, T. J. (2013) · doi:10.1128/9781555819972 · Cited by 3,589 · see citing works
Biofilms as Complex Differentiated Communities
Stoodley, P., Sauer, K., Davies, D. G., & Costerton, J. W. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.160705 · Cited by 3,151 · see citing works
Mechanisms of membrane toxicity of hydrocarbons
Sikkema, J., de Bont, J. A., & Poolman, B. (1995) · Microbiological Reviews · doi:10.1128/mr.59.2.201-222.1995 · Cited by 2,685 · cited 2× · see citing works
“…associated with the presence of these two compounds, as they are documented to cause structural and functional damages to plasma membranes, modifying thus their permeability and leading to leakage of cell contents (Sikkema et al. 1995; Ultee et al. 1999; Lambert et al. 2001; Falcone et al. 2005).”
BackgroundLambert, R. J. W., Skandamis, P. N., Coote, P. J., & Nychas, G.-J. E. (2001) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2001.01428.x · Cited by 2,449 · see citing works
Self-citationLewis, K. (2001) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.45.4.999-1007.2001 · Cited by 1,988 · see citing works
The biofilm matrix – an immobilized but dynamic microbial environment
Sutherland, I. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02012-1 · Cited by 1,269 · see citing works
Mechanisms of Action of Carvacrol on the Food-Borne Pathogen <i>Bacillus cereus</i>
Ultee, A., Kets, E. P. W., & Smid, E. J. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.10.4606-4610.1999 · Cited by 781 · see citing works
Burmølle, M., Webb, J. S., Rao, D., Hansen, L. H., Sørensen, S. J., & Kjelleberg, S. J. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.03022-05 · Cited by 720 · see citing works
Biofilms and their consequences, with particular reference to hygiene in the food industry
Carpentier, B., & Cerf, O. (1993) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1993.tb01587.x · Cited by 603 · see citing works
Chemical Preservatives and Natural Antimicrobial Compounds
Davidson, P. M., Taylor, T. M., & Schmidt, S. E. (2014) · ASM Press eBooks · doi:10.1128/9781555818463.ch30 · Cited by 568 · see citing works
Heterogeneity in biofilms: Table 1
WIMPENNY, J. W. T., Manz, W., & Szewzyk, U. (2000) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2000.tb00565.x · Cited by 530 · see citing works
Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers
Joseph, B., Otta, S. K., Karunasagar, I., & Karunasagar, I. (2001) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(00)00466-9 · Cited by 486 · see citing works
Frank, J. F., & Koffi, R. A. (1990) · Journal of Food Protection · doi:10.4315/0362-028x-53.7.550 · Cited by 430 · see citing works
Microbial biofilms in the food processing industry—Should they be a concern?
Zottola, E. A., & Sasahara, K. C. (1994) · International Journal of Food Microbiology · doi:10.1016/0168-1605(94)90047-7 · Cited by 362 · see citing works
Gibson, H., Taylor, J. H., Hall, K. E., et al. (1999) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1999.00790.x · Cited by 361 · see citing works
Skandamis, P. N., & Nychas, G. E. (2001) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2001.01467.x · Cited by 341 · see citing works
Self-citationNiu, C., & Gilbert, E. S. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.12.6951-6956.2004 · Cited by 331 · see citing works
Biofilms in vitro and in vivo : do singular mechanisms imply cross-resistance?
Gilbert, P., Allison, D., & McBain, A. J. (2002) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.92.5s1.5.x · Cited by 323 · see citing works
Adherence to stainless steel by foodborne microorganisms during growth in model food systems
Hood, S. K., & Zottola, E. A. (1997) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(97)00071-8 · Cited by 286 · see citing works
Antibacterial activity of Turkish spice hydrosols
Sağdıç, O., & Özcan, M. (2003) · Food Control · doi:10.1016/s0956-7135(02)00057-9 · Cited by 259 · see citing works
Knowles, J. R., Roller, S. D., Murray, D. B., et al. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.2.797-803.2005 · Cited by 238 · see citing works
Hood, S. K., & Zottola, E. A. (1995) · Food Control · doi:10.1016/0956-7135(95)91449-u · Cited by 233 · see citing works
Listeria monocytogenes adheres to many materials found in food-processing environments
Beresford, M. R., Andrew, P. W., & Shama, G. (2001) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2001.01330.x · Cited by 231 · see citing works
Carpentier, B., & Chassaing, D. (2004) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2004.03.031 · Cited by 228 · see citing works
Interspecies bacterial interactions in biofilms
James, G. A., Beaudette, L. A., & Costerton, J. W. (1995) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/bf01569978 · Cited by 190 · see citing works
Diez‐Gonzalez, F., & Russell, J. B. (1997) · Microbiology · doi:10.1099/00221287-143-4-1175 · Cited by 168 · see citing works
Leriche, V., & Carpentier, B. (2000) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2000.01000.x · Cited by 146 · see citing works
Control of Listeria monocytogenes in a Biofilm by Competitive-Exclusion Microorganisms
Zhao, T., Doyle, M. P., & Zhao, P. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.7.3996-4003.2004 · Cited by 145 · see citing works
Giaouris, E. D., Chorianopoulos, N., & Nychas, G. E. (2005) · Journal of Food Protection · doi:10.4315/0362-028x-68.10.2149 · Cited by 139 · see citing works
Self-citationAntimicrobials from herbs and spices
Nychas, G. E., Skandamis, P. N., & Tassou, C. C. (2003) · Elsevier eBooks · doi:10.1533/9781855737037.176 · Cited by 136 · see citing works
Self-citationLeriche, V., Briandet, R., & Carpentier, B. (2003) · Environmental Microbiology · doi:10.1046/j.1462-2920.2003.00394.x · Cited by 131 · see citing works
Das, Bhakoo, Jones, & Gilbert (1998) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1998.00422.x · Cited by 129 · see citing works
Biofilm and disinfection in meat processing plants
Jessen, B. H., & Lammert, L. (2003) · International Biodeterioration & Biodegradation · doi:10.1016/s0964-8305(03)00046-5 · Cited by 127 · see citing works
Lactic acid inhibition of the growth of spoilage bacteria and cold tolerant pathogens on pork
GREER, G. G., & Dilts, B. D. (1995) · International Journal of Food Microbiology · doi:10.1016/0168-1605(94)00088-n · Cited by 111 · see citing works
Koutsoumanis, K. P., Lambropoulou, K., & Nychas, G. E. (1999) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(99)00054-9 · Cited by 108 · see citing works
Self-citationGilbert, P., Das, J. R., Jones, M. V., et al. (2001) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2001.01385.x · Cited by 99 · see citing works
Formation of microbial biofilm in hygienic situations: a problem of control
Gilbert, P., McBain, A. J., & Rickard, A. H. (2003) · International Biodeterioration & Biodegradation · doi:10.1016/s0964-8305(03)00043-x · Cited by 94 · see citing works
A Study on the Antimicrobial Activity of Thymol Intended as a Natural Preservative
Falcone, P. M., Speranza, B., Nobile, M. A. D., Corbo, M. R., & Sinigaglia, M. (2005) · Journal of Food Protection · doi:10.4315/0362-028x-68.8.1664 · Cited by 87 · see citing works
Water soluble fractions of rose-scented geranium (Pelargonium species) essential oil
Rao, B. R. R. (2002) · Bioresource Technology · doi:10.1016/s0960-8524(02)00057-3 · Cited by 86 · see citing works
Sommer, P., Martin‐Rouas, C., & Mettler, E. (1999) · Food Microbiology · doi:10.1006/fmic.1999.0267 · Cited by 76 · see citing works
Taormina, P. J., & Beuchat, L. R. (2002) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2002.01488.x · Cited by 73 · see citing works
Leriche, V., Chassaing, D., & Carpentier, B. (1999) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(99)00128-2 · Cited by 71 · see citing works
Lebert, I., Léroy, S., & Talòn, R. (2006) · Food Microbiology · doi:10.1016/j.fm.2006.04.011 · Cited by 69 · see citing works
Chorianopoulos, N., Evergetis, E., Mallouchos, A., Kalpoutzakis, E., Nychas, G. E., & Haroutounian, S. A. (2006) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf053183n · Cited by 67 · see citing works
Self-citationBacterial behavior at surfaces
Geesey, G. G. (2001) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00206-x · Cited by 62 · see citing works
BIOFILM ANTIMICROBIAL RESISTANCE
Stewart, P. S., Mukherjee, P. K., & Ghannoum, M. A. (2004) · doi:10.1128/9781555817718.ch14 · Cited by 57 · see citing works
Gören, A. C., Topçu, G., Bilsel, G., et al. (2004) · Natural Product Research · doi:10.1080/14786410310001608145 · Cited by 55 · see citing works
Roller, S. D. (1995) · International Biodeterioration & Biodegradation · doi:10.1016/0964-8305(95)00074-7 · Cited by 50 · see citing works
Gawande, P. V., & Bhagwat, A. A. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.1.86-92.2002 · Cited by 43 · see citing works
Al-Shuneigat, J., Cox, S. D., & Markham, J. L. (2005) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2005.01699.x · Cited by 40 · see citing works
Costerton, J. W. (1995) · Annual Review of Microbiology · doi:10.1146/annurev.micro.49.1.711 · Cited by 40 · see citing works
Ammor, S., Chevallier, I., Laguet, A., Labadie, J., Talòn, R., & Dufour, É. (2003) · Food Microbiology · doi:10.1016/s0740-0020(03)00051-0 · Cited by 28 · see citing works
Flint, S., Brooks, J. D., & Bremer, P. J. (1997) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1997.00233.x · Cited by 26 · see citing works
MICROBIAL INTERACTIONS IN MIXED‐SPECIES BIOFILMS
Molin, S., Tolker‐Nielsen, T., & Hansen, S. K. (2004) · doi:10.1128/9781555817718.ch12 · Cited by 7 · see citing works
Gilbert, P., Das, J., Jones, M. N., et al. (2001) · Research Explorer (The University of Manchester) · Cited by 5 · see citing works
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Effect of essential oils on pathogenic bacteria
Nazzaro, F., Fratianni, F., De Martino, L., Coppola, R., & De Feo, V. (2013) · Pharmaceuticals · doi:10.3390/ph6121451 · Cited by 2,186 · see citing works
“Most EOs have a more powerful effect on Gram-positive bacteria than Gram-negative species, and this effect is most likely due to differences in the cell membrane compositions (Figure 1) [3,56,58].”
BackgroundApplication of natural antimicrobials for food preservation
Tiwari, B. K., Valdramidis, V. P., O’ Donnell, C. P., Muthukumarappan, K., Bourke, P., & Cullen, P. J. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf900668n · Cited by 851 · see citing works
Aćimović, M., Tešević, V., Smiljanić, K., Cvetković, M., Stanković, J., Kiprovski, B., & Sikora, V. (2020) · Advanced Technologies · doi:10.5937/savteh2002054a · Cited by 121 · see citing works
- Authors
- Chorianopoulos, N. G., Giaouris, E. D., Skandamis, P. N., Haroutounian, S. A., & Nychas, G.-J. E.
- Affiliations
- Agricultural University of Athens (GR)
- Corresponding author
- Giaouris, E.D.
- Venue
- Journal of Applied Microbiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-06
- Volume
- 104
- Issue
- 6
- Pages
- 1586-1596
- ISSN
- 1364-5072 (ISSN-L)
- 1365-2672
- OpenAlex
- W1973191374
- Cited by
- 202
- References
- 57
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 5 · 2023: 15 · 2022: 17 · 2021: 13 · 2020: 12 · 2019: 15 · 2018: 11 · 2017: 18 · 2016: 11 · 2015: 15 · 2014: 8 · 2013: 13 · 2012: 15
- FWCI
- 12.80
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Essential Oils and Antimicrobial Activity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Physical Sciences › Chemistry › Organic Chemistry › Antimicrobial agents and applications
- Keywords
- Satureja thymbra, essential oils, hydrosols, biofilm disinfection, mixed-culture biofilms, natural antimicrobials, stainless steel surfaces, Staphylococcus simulans, Lactobacillus fermentum, Pseudomonas putida, Salmonella enterica, Listeria monocytogenes, bactericidal activity
- MeSH terms
- Bacteria, Disinfectants, Disinfection, Equipment Contamination, Humans, Hydrochloric Acid, Hydrogen-Ion Concentration, Industrial Microbiology, Oils, Volatile, Stainless Steel, Biofilms, Lactic Acid, Hydrogels, Plant Preparations, Satureja
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