Bacterial Inactivation by Using Plastic Materials Activated with Combinations of Natural Antimicrobials
Abstract
:1. Introduction
2. Materials and Methods
2.1. Activation of Plastic Squares
2.2. Effect of Activated Films on Planktonic and Sessile Viable Cell Concentrations
2.3. Statistical Analysis
3. Results
4. Discussion
Author Contributions
Funding
Conflicts of Interest
References
- Branda, S.S.; Vik, A.; Friedman, L.; Kolter, R. Biofilms: The matrix revisited. Trends Microbiol. 2005, 13, 20–26. [Google Scholar] [CrossRef] [PubMed]
- Van Houdt, R.; Michiels, C.W. Biofilm formation and the food industry, a focus on the bacterial outer surface. J. Appl. Microbiol. 2010, 109, 1117–1131. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Davey, M.E.; O’toole, G.A. Microbial biofilms: From ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 2000, 64, 847–867. [Google Scholar] [CrossRef] [PubMed]
- Stoodley, P.; Sauer, K.; Davies, D.G.; Costerton, J.W. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 2002, 56, 187–209. [Google Scholar] [CrossRef] [PubMed]
- Coughlan, L.M.; Cotter, P.D.; Hill, C.; Alvarez-Ordóñez, A. New weapons to fight old enemies: Novel strategies for the (bio)control of bacterial biofilms in the food industry. Front. Microbiol. 2016, 7, 1641. [Google Scholar] [CrossRef] [PubMed]
- Gutiérrez, D.; Rodríguez-Rubio, L.; Martínez, B.; Rodríguez, A.; García, P. Bacteriophages as weapons against bacterial biofilms in the food industry. Front. Microbiol. 2016, 7, 825. [Google Scholar] [CrossRef] [PubMed]
- Sadekuzzaman, M.; Yang, S.; Mizan, M.F.R.; Ha, S.D. Current and recent advanced strategies for combating biofilms. Compr. Rev. Food Sci. Food Saf. 2015, 14, 491–509. [Google Scholar] [CrossRef]
- Jack, R.W.; Tagg, J.R.; Ray, B. Bacteriocins of gram-positive bacteria. Microbiol. Rev. 1995, 59, 171–200. [Google Scholar] [PubMed]
- Cleveland, J.; Montville, T.J.; Nes, I.F.; Chikindas, M.L. Bacteriocins: Safe, natural antimicrobials for food preservation. Int. J. Food Microbiol. 2001, 71, 1–20. [Google Scholar] [CrossRef]
- Deegan, L.H.; Cotter, P.D.; Hill, C.; Ross, P. Bacteriocins: Biological tools for bio-preservation and shelf-life extension. Int. Dairy J. 2006, 16, 1058–1071. [Google Scholar] [CrossRef]
- Gálvez, A.; Abriouel, H.; López, R.L.; Ben Omar, N. Bacteriocin-based strategies for food biopreservation. Int. J. Food Microbiol. 2007, 120, 51–70. [Google Scholar] [CrossRef] [PubMed]
- Galvez, A.M.; Grande Burgos, M.J.; Lucas Lopez, R.; Pérez Pulido, R. Food Biopreservation; Springer: New York, NY, USA, 2014. [Google Scholar]
- Abriouel, H.; Lucas, R.; Omar, N.B.; Valdivia, E.; Gálvez, A. Potential applications of the cyclic peptide enterocin AS-48 in the preservation of vegetable foods and beverages. Probiotics Antimicrob. Proteins. 2010, 2, 77–89. [Google Scholar] [CrossRef] [PubMed]
- Grande-Burgos, M.J.; Pulido, R.P.; López-Aguayo, M.D.C.; Gálvez, A.; Lucas, R. The cyclic antibacterial peptide enterocin AS-48: Isolation, mode of action, and possible food applications. Int. J. Mol. Sci. 2014, 15, 22706–22727. [Google Scholar] [CrossRef] [PubMed]
- Vargas, M.; Pastor, C.; Chiralt, A.; McClements, D.J.; Gonzalez-Martínez, C. Recent advances in edible coatings for fresh and minimally processed fruits. Crit. Rev. Food Sci. Nutr. 2018, 48, 496–511. [Google Scholar] [CrossRef] [PubMed]
- Sung, S.-Y.; Sin, L.T.; Tee, T.T.; Bee, S.-T.; Rahmat, A.R.; Rahman, W.A.W.A.; Tan, A.-C.; Vikhraman, M. Antimicrobial agents for food packaging applications. Trends Food Sci. Technol. 2013, 33, 110–123. [Google Scholar] [CrossRef]
- Bazaka, K.; Jacob, M.V.; Crawford, R.J.; Ivanova, E.P. Efficient surface modification of biomaterial to prevent biofilm formation and the attachment of microorganisms. Appl. Microbiol. Biotechnol. 2012, 95, 299–311. [Google Scholar] [CrossRef] [PubMed]
- Burt, S.A.; Ojo-Fakunle, V.T.A.; Woertman, J.; Veldhuizen, E.J.A. The natural antimicrobial carvacrol inhibits quorum sensing in Chromobacterium violaceum and reduces bacterial biofilm formation at sub-lethal concentrations. PLoS ONE 2014, 9, e93414. [Google Scholar] [CrossRef]
- Nostro, A.; Scaffaro, R.; D’Arrigo, M.; Botta, L.; Filocamo, A.; Marino, A.; Bisignani, G. Study on carvacrol and cinnamaldehyde polymeric films: Mechanical properties, release kinetics and antibacterial and antibiofilm activities. Appl. Microbiol. Biotechnol. 2012, 96, 1029–1038. [Google Scholar] [CrossRef] [PubMed]
- Gómez, N.C.; Abriouel, H.; Grande, M.A.; Pulido, R.P.; Gálvez, A. Effect of enterocin AS-48 in combination with biocides on planktonic and sessile Listeria monocytogenes. Food Microbiol. 2012, 30, 51–58. [Google Scholar] [CrossRef]
- Gómez, N.C.; Grande, M.J.; Pulido, R.P.; Abriouel, H.; Gálvez, A. Effect of enterocin AS-48 singly or in combination with biocides on planktonic and sessile B. cereus. Food Cont. 2013, 34, 743–751. [Google Scholar] [CrossRef]
- Abriouel, H.; Valdivia, E.; Martínez-Bueno, M.; Maqueda, M.; Gálvez, A. A simple method for semi-preparative-scale production and recovery of enterocin AS-48 derived from Enterococcus faecalis subsp. liquefaciens A-48-32. J. Microbiol. Meth. 2003, 55, 599–605. [Google Scholar] [CrossRef]
- Hyldgaard, M.; Mygind, T.; Meyer, R.L. Essential oils in food preservation: Mode of action, synergies, and interactions with food matrix components. Front Microbiol. 2012, 3, 12. [Google Scholar] [CrossRef]
- Mendoza, F.; Maqueda, M.; Gálvez, A.; Martínez-Bueno, M.; Valdivia, E. Antilisterial activity of peptide AS-48 and study of changes induced in the cell envelope properties of an AS-48-adapted strain of Listeria monocytogenes. Appl. Environ. Microbiol. 1999, 65, 618–625. [Google Scholar] [PubMed]
- Srey, S.; Jahid, I.K.; Ha, S.-D. Biofilm formation in food industries: A food safety concern. Food Cont. 2013, 31, 572–585. [Google Scholar] [CrossRef]
- Winkelströter, L.K.; Gomes, B.C.; Thomaz, M.R.S.; Souza, V.M.; De Martinis, E.C.P. Lactobacillus sakei 1 and its bacteriocin influence adhesion of Listeria monocytogenes on stainless steel surface. Food Cont. 2011, 22, 1404–1407. [Google Scholar] [CrossRef]
- Sudagidan, M.; Yemenicioğlu, A. Effects of nisin and lysozyme on growth inhibition and biofilm formation capacity of Staphylococcus aureus strains isolated from raw milk and cheese samples. J. Food Prot. 2012, 75, 1627–1633. [Google Scholar] [CrossRef] [PubMed]
- Bolocan, A.S.; Pennone, V.; O’Connor, P.M.; Coffey, A.; Nicolau, A.I.; McAuliffe, O.; Jordan, K. Inhibition of Listeria monocytogenes biofilms by bacteriocin-producing bacteria isolated from mushroom substrate. J. Appl. Microbiol. 2017, 122, 279–293. [Google Scholar] [CrossRef]
- Camargo, A.C.; De Paula, O.A.; Todorov, S.D.; Nero, L.A. In Vitro Evaluation of bacteriocins activity against Listeria monocytogenes biofilm formation. Appl. Biochem. Biotechnol. 2016, 178, 1239–1251. [Google Scholar] [CrossRef]
- Pérez-Conesa, D.; McLandsborough, L.; Weiss, J. Inhibition and inactivation of Listeria monocytogenes and Escherichia coli O157:H7 colony biofilms by micellar-encapsulated eugenol and carvacrol. J. Food Prot. 2006, 69, 2947–2954. [Google Scholar] [CrossRef]
- Nostro, A.; Sudano Roccaro, A.; Bisignano, G.; Marino, A.; Cannatelli, M.A.; Pizzimenti, F.C.; Cioni, P.L.; Procopio, F.; Blanco, A.R. Effects of oregano, carvacrol and thymol on Staphylococcus aureus and Staphylococcus epidermidis biofilms. J. Med. Microbiol. 2007, 56, 519–523. [Google Scholar] [CrossRef]
- Karpanen, T.J.; Worthington, T.; Hendry, E.R.; Conway, B.R.; Lambert, P.A. Antimicrobial efficacy of chlorhexidine digluconate alone and in combination with eucalyptus oil, tea tree oil and thymol against planktonic and biofilm cultures of Staphylococcus epidermidis. J. Antimicrob. Chemother. 2008, 62, 1031–1036. [Google Scholar] [CrossRef] [PubMed]
- Soni, K.A.; Oladunjoye, A.; Nannapeneni, R.; Schilling, M.W.; Silva, J.L.; Mikel, B.; Bailey, R.H. Inhibition and inactivation of Salmonella Typhimurium biofilms from polystyrene and stainless steel surfaces by essential oils and phenolic constituent carvacrol. J. Food Prot. 2013, 67, 205–212. [Google Scholar] [CrossRef] [PubMed]
- Upadhyaya, I.; Upadhyay, A.; Kollanoor-Johny, A.; Baskaran, S.A.; Mooyottu, S.; Darre, M.J.; Venkitanarayanan, K. Rapid inactivation of Salmonella enteritidis on shell eggs by plant-derived antimicrobials. Poult. Sci. 2013, 92, 3228–3235. [Google Scholar] [CrossRef]
- Knowles, J.R.; Roller, S.; Murray, D.B.; Naidu, A.S. Antimicrobial action of carvacrol at different stages of dual-species biofilm development by Staphylococcus aureus and Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 2005, 71, 797–803. [Google Scholar] [CrossRef] [PubMed]
- Niu, C.; Afre, S.; Gilbert, E.S. Subinhibitory concentrations of cinnamaldehyde interfere with quorum sensing. Lett. Appl. Microbiol. 2006, 43, 489–494. [Google Scholar] [CrossRef] [PubMed][Green Version]
Bacteria and Treatment | Planktonic Cells (log CFU/mL) | Sessile Cells (log CFU/cm2) | ||||
---|---|---|---|---|---|---|
24 h | 48 h | 72 h | 24 h | 48 h | 72 h | |
Listeria innocua | ||||||
LDPEC | 9.17 ± 0.07 | 9.32 ± 0.03 | 8.82 ± 0.04 | 7.94 ± 0.17 | 7.93 ± 0.22 | 7.86 ± 0.12 |
LDPECvc-AS-48 | <1.0 † | <1.0 † | <1.0 † | <1.11 † | 2.90 ± 0.34 † | <1.11 † |
LDPEThy-AS-48 | <1.0 † | <1.0 † | <1.0 † | <1.11 † | 2.60 ± 0.05 † | <1.11 † |
PEAC | 8.91 ± 0.10 | 8.92 ± 0.18 | 8.85 ± 0.10 | 8.22 ± 0.31 | 7.97 ± 0.17 | 8.03 ± 0.19 |
PEACvc-AS-48 | <1.0 † | 2.38 ± 0.15 † | <1.0 † | <1.11 † | 3.88 ± 0.08 † | <1.11 † |
PEAThy-AS-48 | <1.0 † | <1.0 † | <1.0 † | <1.11 † | <1.11 † | <1.11 † |
Lactobacillus fructivorans | ||||||
LDPEC | 7.51 ± 0.15 | 8.45 ± 0.07 | 9.51 ± 0.18 | 4.88 ± 0.08 | 5.77 ± 0.22 | 5.41 ± 0.27 |
LDPECvc-AS-48 | 3.34 ± 0.13 † | 4.15 ± 0.21 † | 5.50 ± 0.17 † | <1.11 † | <1.11 † | 2.70 ± 0.36 † |
LDPEThy-AS-48 | 3.50 ± 0.20 † | 3.54 ± 0.20 † | 4.48 ± 0.28 † | <1.11 † | <1.11 † | 2.42 ± 0.28 † |
PEAC | 7.78 ± 0.11 | 8.56 ± 0.18 | 9.45 ± 0.07 | 5.33 ± 0.21 | 6.89 ± 0.32 | 7.41 ± 0.37 |
PEACvc-AS-48 | <1.0 † | 3.48 ± 0.15 † | 5.47 ± 0.18 † | <1.11 † | <1.11 † | 2.89 ± 0.46 † |
PEAThy-AS-48 | <1.0 † | 3.50 ± 0.14 | 4.47 ± 0.10 | <1.11 † | <1.11 † | 3.73 ± 0.25 † |
Bacillus coagulans | ||||||
LDPEC | 6.12 ± 0.17 | 8.19 ± 0.27 | 8.30 ± 0.12 | 4.03 ± 0.19 | 6.62 ± 0.25 | 6.98 ± 0.28 |
LDPECvc-AS-48 | 2.47 ± 0.07 † | 1.30 ± 0.14 † | 2.20 ± 0.24 † | 1.88 ± 0.20 † | <1.11 † | <1.11 † |
LDPEThy-AS-48 | 4.93 ± 0.23 † | 4.46 ± 0.23 † | 3.32 ± 0.21 † | 3.52 ± 0.32 | <1.11 † | 1.11 ± 0.19 † |
PEAC | 6.00 ± 0.16 | 8.35 ± 0.21 | 8.11 ± 0.16 | 5.95 ± 0.14 | 8.27 ± 0.18 | 8.97 ± 0.28 |
PEACvc-AS-48 | <1.0 † | 1.48 ± 0.25 † | 1.60 ± 0.27 † | <1.11 † | 2.04 ± 0.22 † | <1.11 † |
PEAThy-AS-48 | <1.0 † | <1.0 † | <1.0 † | <1.11 † | <1.11 † | <1.11 † |
Bacillus licheniformis | ||||||
LDPEC | 3.0 ± 0.08 | 5.93 ± 0.14 | 6.40 ± 0.19 | 2.17 ± 0.20 | 4.34 ± 0.17 | 4.75 ± 0.28 |
LDPECvc-AS-48 | <1.0 † | 1.48 ± 0.11 † | <1.0 † | <1.11 † | <1.11 † | <1.11 † |
LDPEThy-AS-48 | <1.0 † | <1.0 † | <1.0 † | <1.11 † | <1.11 † | <1.11 † |
PEAC | 3.70 ± 0.19 | 6.65 ± 0.18 | 7.22 ± 0.31 | 1.96 ± 0.10 | 5.53 ± 0.28 | 5.40 ± 0.25 |
PEACvc-AS-48 | <1.0 † | <1.0 † | <1.0 † | <1.11 † | <1.11 † | <1.11 † |
PEAThy-AS-48 | <1.0 † | <1.0 † | <1.0 † | <1.11 † | <1.11 † | <1.11 † |
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ortega Blázquez, I.; Grande Burgos, M.J.; Pérez Pulido, R.; Gálvez, A.; Lucas, R. Bacterial Inactivation by Using Plastic Materials Activated with Combinations of Natural Antimicrobials. Coatings 2018, 8, 460. https://doi.org/10.3390/coatings8120460
Ortega Blázquez I, Grande Burgos MJ, Pérez Pulido R, Gálvez A, Lucas R. Bacterial Inactivation by Using Plastic Materials Activated with Combinations of Natural Antimicrobials. Coatings. 2018; 8(12):460. https://doi.org/10.3390/coatings8120460
Chicago/Turabian StyleOrtega Blázquez, Irene, María José Grande Burgos, Rubén Pérez Pulido, Antonio Gálvez, and Rosario Lucas. 2018. "Bacterial Inactivation by Using Plastic Materials Activated with Combinations of Natural Antimicrobials" Coatings 8, no. 12: 460. https://doi.org/10.3390/coatings8120460