Natural Plant-Derived Chemical Compounds as Listeria monocytogenes Inhibitors In Vitro and in Food Model Systems
Abstract
:1. Listeria Monocytogenes
2. Antilisterial Plant-Derived Compounds
3. Mechanisms of Action
3.1. Gene Expression Responses and Proteome Changes
3.2. Bacterial Adaptation
3.3. Virulence in In Vitro and In Vivo Models
4. Food Model Systems
5. Combining NPDA and Other Antilisterial Factors
5.1. Plant Antimicrobials Used in Combination
5.2. Bacteriocins
5.3. Heat Treatments
5.4. Antibiotics
5.5. Other Factors
6. Alternative Delivery Methods of the Components Used against L. monocytogenes
7. Natural Substances against L. monocytogenes Biofilm
8. Summary and Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Bintsis, T. Foodborne pathogens. AIMS Microbiol. 2017, 3, 529–563. [Google Scholar] [CrossRef]
- Gandhi, M.; Chikindas, M.L. Listeria: A foodborne pathogen that knows how to survive. Int. J. Food Microbiol. 2007, 113, 1–15. [Google Scholar] [CrossRef]
- Lecuit, M. Human listeriosis and animal models. Microbes Infect. 2007, 9, 1216–1225. [Google Scholar] [CrossRef]
- Radoshevich, L.; Cossart, P. Listeria monocytogenes: Towards a complete picture of its physiology and pathogenesis. Nat. Rev. Microbiol. 2018, 16, 32–46. [Google Scholar] [CrossRef] [PubMed]
- Vázquez-Boland, J.A.; Kuhn, M.; Berche, P.; Chakraborty, T.; Domínguez-Bernal, G.; Goebel, W.; González-Zorn, B.; Wehland, J.; Kreft, J. Listeria Pathogenesis and Molecular Virulence Determinants. Clin. Microbiol. Rev. 2001, 14, 584–640. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, Q.; Gooneratne, R.; Hussain, M.A. Listeria monocytogenes in Fresh Produce: Outbreaks, Prevalence and Contamination Levels. Foods 2017, 6, 21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gray, J.A.; Chandry, P.S.; Kaur, M.; Kocharunchitt, C.; Bowman, J.P.; Fox, E.M. Novel Biocontrol Methods for Listeria monocytogenes Biofilms in Food Production Facilities. Front. Microbiol. 2018, 9, 605. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jami, M.; Ghanbari, M.; Zunabovic, M.; Domig, K.J.; Kneifel, W. Listeria monocytogenes in Aquatic Food Products—A Review. Compr. Rev. Food Sci. Food Saf. 2014, 13, 798–813. [Google Scholar] [CrossRef]
- Jordan, K.; McAuliffe, O. Listeria monocytogenes in Foods. In Advances in Food and Nutrition Research; Academic Press: Cambridge, MA, USA, 2018; Volume 86, pp. 181–213. ISBN 978-0-12-813977-6. [Google Scholar]
- Barbieri, R.; Coppo, E.; Marchese, A.; Daglia, M.; Sobarzo-Sánchez, E.; Nabavi, S.F.; Nabavi, S.M. Phytochemicals for human disease: An update on plant-derived compounds antibacterial activity. Microbiol. Res. 2017, 196, 44–68. [Google Scholar] [CrossRef] [PubMed]
- Chai, T.-T.; Tan, Y.-N.; Ee, K.-Y.; Xiao, J.; Wong, F.-C. Seeds, fermented foods, and agricultural by-products as sources of plant-derived antibacterial peptides. Crit. Rev. Food Sci. Nutr. 2019, 59, S162–S177. [Google Scholar] [CrossRef]
- Kokoska, L.; Kloucek, P.; Leuner, O.; Novy, P. Plant-Derived Products as Antibacterial and Antifungal Agents in Human Health Care. Curr. Med. Chem. 2019, 26, 5501–5541. [Google Scholar] [CrossRef] [PubMed]
- Burt, S. Essential oils: Their antibacterial properties and potential applications in foods—A review. Int. J. Food Microbiol. 2004, 94, 223–253. [Google Scholar] [CrossRef] [PubMed]
- Fisher, K.; Phillips, C. Potential antimicrobial uses of essential oils in food: Is citrus the answer? Trends Food Sci. Technol. 2008, 19, 156–164. [Google Scholar] [CrossRef]
- Pandey, A.K.; Kumar, P.; Singh, P.; Tripathi, N.N.; Bajpai, V.K. Essential Oils: Sources of Antimicrobials and Food Preservatives. Front. Microbiol. 2017, 7, 2161. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sakkas, H.; Papadopoulou, C. Antimicrobial Activity of Basil, Oregano, and Thyme Essential Oils. J. Microbiol. Biotechnol. 2017, 27, 429–438. [Google Scholar] [CrossRef] [Green Version]
- Dhifi, W.; Jazi, S.; El Beyrouthy, M.; Sadaka, C.; Mnif, W. Assessing the potential and safety of Myrtus communis flower essential oils as efficient natural preservatives against Listeria monocytogenes growth in minced beef under refrigeration. Food Sci. Nutr. 2020, 8, 2076–2087. [Google Scholar] [CrossRef] [Green Version]
- Vergis, J.; Gokulakrishnan, P.; Agarwal, R.K.; Kumar, A. Essential oils as natural food antimicrobial agents: A review. Crit. Rev. Food Sci. Nutr. 2015, 55, 1320–1323. [Google Scholar] [CrossRef]
- Falleh, H.; Ben Jemaa, M.; Saada, M.; Ksouri, R. Essential oils: A promising eco-friendly food preservative. Food Chem. 2020, 330, 127268. [Google Scholar] [CrossRef]
- Wińska, K.; Mączka, W.; Łyczko, J.; Grabarczyk, M.; Czubaszek, A.; Szumny, A. Essential Oils as Antimicrobial Agents—Myth or Real Alternative? Molecules 2019, 24, 2130. [Google Scholar] [CrossRef] [Green Version]
- de Groot, A.C.; Schmidt, E. Essential Oils, Part III: Chemical Composition. Dermatitis 2016, 27, 161–169. [Google Scholar] [CrossRef]
- Friedman, M.; Henika, P.R.; Mandrell, R.E. Bactericidal activities of plant essential oils and some of their isolated constituents against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. J. Food Prot. 2002, 65, 1545–1560. [Google Scholar] [CrossRef] [PubMed]
- Pol, I.E.; Smid, E.J. Combined action of nisin and carvacrol on Bacillus cereus and Listeria monocytogenes. Lett. Appl. Microbiol. 1999, 29, 166–170. [Google Scholar] [CrossRef] [PubMed]
- Brnawi, W.I.; Hettiarachchy, N.S.; Horax, R.; Kumar-Phillips, G.; Seo, H.-S.; Marcy, J. Comparison of Cinnamon Essential Oils from Leaf and Bark with Respect to Antimicrobial Activity and Sensory Acceptability in Strawberry Shake. J. Food Sci. 2018, 83, 475–480. [Google Scholar] [CrossRef]
- Carvalho, M.I.P.; Albano, H.C.P.; Teixeira, P.C.M. Influence of oregano essential oil on the inhibition of selected pathogens in “Alheira” during storage. Acta Sci. Pol. Technol. Aliment. 2019, 18, 13–23. [Google Scholar] [CrossRef] [PubMed]
- Cho, Y.; Kim, H.; Beuchat, L.R.; Ryu, J.-H. Synergistic activities of gaseous oregano and thyme thymol essential oils against Listeria monocytogenes on surfaces of a laboratory medium and radish sprouts. Food Microbiol. 2020, 86, 103357. [Google Scholar] [CrossRef]
- Guedes, J.P.d.S.; de Souza, E.L. Investigation of damage to Escherichia coli, Listeria monocytogenes and Salmonella Enteritidis exposed to Mentha arvensis L. and M. piperita L. essential oils in pineapple and mango juice by flow cytometry. Food Microbiol. 2018, 76, 564–571. [Google Scholar] [CrossRef]
- Iseppi, R.; Camellini, S.; Sabia, C.; Messi, P. Combined antimicrobial use of essential oils and bacteriocin bacLP17 as seafood biopreservative to control Listeria monocytogenes both in planktonic and in sessile forms. Res. Microbiol. 2020, 171, 351–356. [Google Scholar] [CrossRef]
- Kang, J.-H.; Song, K.B. Combined effect of a positively charged cinnamon leaf oil emulsion and organic acid on the inactivation of Listeria monocytogenes inoculated on fresh-cut Treviso leaves. Food Microbiol. 2018, 76, 146–153. [Google Scholar] [CrossRef]
- Lee, G.; Kim, Y.; Kim, H.; Beuchat, L.R.; Ryu, J.-H. Antimicrobial activities of gaseous essential oils against Listeria monocytogenes on a laboratory medium and radish sprouts. Int. J. Food Microbiol. 2018, 265, 49–54. [Google Scholar] [CrossRef]
- Lorenzo-Leal, A.C.; Palou, E.; López-Malo, A. Evaluation of the efficiency of allspice, thyme and rosemary essential oils on two foodborne pathogens in in vitro and on alfalfa seeds, and their effect on sensory characteristics of the sprouts. Int. J. Food Microbiol. 2019, 295, 19–24. [Google Scholar] [CrossRef]
- Mortazavi, N.; Aliakbarlu, J. Antibacterial Effects of Ultrasound, Cinnamon Essential Oil, and Their Combination against Listeria monocytogenes and Salmonella Typhimurium in Milk. J. Food Sci. 2019, 84, 3700–3706. [Google Scholar] [CrossRef] [PubMed]
- Shi, C.; Zhang, X.; Guo, N. The antimicrobial activities and action-mechanism of tea tree oil against food-borne bacteria in fresh cucumber juice. Microb. Pathog. 2018, 125, 262–271. [Google Scholar] [CrossRef] [PubMed]
- Silva, C.d.S.; de Figueiredo, H.M.; Stamford, T.L.M.; da Silva, L.H.M. Inhibition of Listeria monocytogenes by Melaleuca alternifolia (tea tree) essential oil in ground beef. Int. J. Food Microbiol. 2019, 293, 79–86. [Google Scholar] [CrossRef] [PubMed]
- Siroli, L.; Baldi, G.; Soglia, F.; Bukvicki, D.; Patrignani, F.; Petracci, M.; Lanciotti, R. Use of Essential Oils to Increase the Safety and the Quality of Marinated Pork Loin. Foods 2020, 9, 987. [Google Scholar] [CrossRef] [PubMed]
- Anastasiadi, M.; Chorianopoulos, N.G.; Nychas, G.-J.E.; Haroutounian, S.A. Antilisterial activities of polyphenol-rich extracts of grapes and vinification byproducts. J. Agric. Food Chem. 2009, 57, 457–463. [Google Scholar] [CrossRef] [PubMed]
- Park, Y.J.; Biswas, R.; Phillips, R.D.; Chen, J. Antibacterial activities of blueberry and muscadine phenolic extracts. J. Food Sci. 2011, 76, M101–M105. [Google Scholar] [CrossRef]
- Rhodes, P.; Mitchell, J.; Wilson, M.; Melton, L. Antilisterial activity of grape juice and grape extracts derived from Vitis vinifera variety Ribier. Int. J. Food Microbiol. 2006, 107, 281–286. [Google Scholar] [CrossRef]
- Lacombe, A.; Wu, V.C.H.; White, J.; Tadepalli, S.; Andre, E.E. The antimicrobial properties of the lowbush blueberry (Vaccinium angustifolium) fractional components against foodborne pathogens and the conservation of probiotic Lactobacillus rhamnosus. Food Microbiol. 2012, 30, 124–131. [Google Scholar] [CrossRef]
- Friedman, M.; Henika, P.R.; Levin, C.E. Bactericidal activities of health-promoting, food-derived powders against the foodborne pathogens Escherichia coli, Listeria monocytogenes, Salmonella enterica, and Staphylococcus aureus. J. Food Sci. 2013, 78, M270–M275. [Google Scholar] [CrossRef]
- Yu, H.H.; Song, M.W.; Song, Y.J.; Lee, N.-K.; Paik, H.-D. Antibacterial Effect of a Mixed Natural Preservative against Listeria monocytogenes on Lettuce and Raw Pork Loin. J. Food Prot. 2019, 82, 2001–2006. [Google Scholar] [CrossRef]
- Benedec, D.; Hanganu, D.; Oniga, I.; Filip, L.; Bischin, C.; Silaghi-Dumitrescu, R.; Tiperciuc, B.; Vlase, L. Achillea schurii Flowers: Chemical, Antioxidant, and Antimicrobial Investigations. Molecules 2016, 21, 1050. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lis-Balchin, M.; Deans, S.G. Bioactivity of selected plant essential oils against Listeria monocytogenes. J. Appl. Microbiol. 1997, 82, 759–762. [Google Scholar] [CrossRef] [PubMed]
- Liang, Y.; Li, Y.; Sun, A.; Liu, X. Chemical compound identification and antibacterial activity evaluation of cinnamon extracts obtained by subcritical N-butane and ethanol extraction. Food Sci. Nutr. 2019, 7, 2186–2193. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kobayashi, Y.; Sato, H.; Yorita, M.; Nakayama, H.; Miyazato, H.; Sugimoto, K.; Jippo, T. Inhibitory effects of geranium essential oil and its major component, citronellol, on degranulation and cytokine production by mast cells. Biosci. Biotechnol. Biochem. 2016, 80, 1172–1178. [Google Scholar] [CrossRef] [Green Version]
- Ma, B.; Ban, X.; Huang, B.; He, J.; Tian, J.; Zeng, H.; Chen, Y.; Wang, Y. Interference and Mechanism of Dill Seed Essential Oil and Contribution of Carvone and Limonene in Preventing Sclerotinia Rot of Rapeseed. PLoS ONE 2015, 10, e0131733. [Google Scholar] [CrossRef] [Green Version]
- Viktorová, J.; Stupák, M.; Řehořová, K.; Dobiasová, S.; Hoang, L.; Hajšlová, J.; Van Thanh, T.; Van Tri, L.; Van Tuan, N.; Ruml, T. Lemon Grass Essential Oil does not Modulate Cancer Cells Multidrug Resistance by Citral—Its Dominant and Strongly Antimicrobial Compound. Foods 2020, 9, 585. [Google Scholar] [CrossRef]
- Chaieb, K.; Hajlaoui, H.; Zmantar, T.; Kahla-Nakbi, A.B.; Rouabhia, M.; Mahdouani, K.; Bakhrouf, A. The chemical composition and biological activity of clove essential oil, Eugenia caryophyllata (Syzigium aromaticum L. Myrtaceae): A short review. Phytother. Res. 2007, 21, 501–506. [Google Scholar] [CrossRef]
- Białoń, M.; Krzyśko-Łupicka, T.; Nowakowska-Bogdan, E.; Wieczorek, P.P. Chemical Composition of Two Different Lavender Essential Oils and Their Effect on Facial Skin Microbiota. Molecules 2019, 24, 3270. [Google Scholar] [CrossRef] [Green Version]
- Paniandy, J.-C.; Chane-Ming, J.; Pieribattesti, J.-C. Chemical Composition of the Essential Oil and Headspace Solid-Phase Microextraction of the Guava Fruit (Psidium guajava L.). J. Essent. Oil Res. 2000, 12, 153–158. [Google Scholar] [CrossRef]
- Bagheri, L.; Khodaei, N.; Salmieri, S.; Karboune, S.; Lacroix, M. Correlation between chemical composition and antimicrobial properties of essential oils against most common food pathogens and spoilers: In vitro efficacy and predictive modelling. Microb. Pathog. 2020, 147, 104212. [Google Scholar] [CrossRef]
- Periago, P.M.; Delgado, B.; Fernández, P.S.; Palop, A. Use of carvacrol and cymene to control growth and viability of Listeria monocytogenes cells and predictions of survivors using frequency distribution functions. J. Food Prot. 2004, 67, 1408–1416. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Niu, H.; Zhang, W.; Mu, H.; Sun, C.; Duan, J. Synergy among thymol, eugenol, berberine, cinnamaldehyde and streptomycin against planktonic and biofilm-associated food-borne pathogens. Lett. Appl. Microbiol. 2015, 60, 421–430. [Google Scholar] [CrossRef] [PubMed]
- Karatzas, A.K.; Bennik, M.H.; Smid, E.J.; Kets, E.P. Combined action of S-carvone and mild heat treatment on Listeria monocytogenes Scott A. J. Appl. Microbiol. 2000, 89, 296–301. [Google Scholar] [CrossRef] [PubMed]
- Dias, C.; Aires, A.; Bennett, R.N.; Rosa, E.A.S.; Saavedra, M.J. First study on antimicriobial activity and synergy between isothiocyanates and antibiotics against selected Gram-negative and Gram-positive pathogenic bacteria from clinical and animal source. Med. Chem. 2012, 8, 474–480. [Google Scholar] [CrossRef] [PubMed]
- Hakkim, F.L.; Essa, M.M.; Arivazhagan, G.; Guizani, N.; Hyuk, S. Evaluation of food protective property of five natural products using fresh-cut apple slice model. Pak. J. Biol. Sci. 2012, 15, 10–18. [Google Scholar] [CrossRef] [PubMed]
- Alves, F.C.B.; Barbosa, L.N.; Andrade, B.F.M.T.; Albano, M.; Furtado, F.B.; Pereira, A.F.M.; Rall, V.L.M.; Júnior, A.F. Inhibitory activities of the lantibiotic nisin combined with phenolic compounds against Staphylococcus aureus and Listeria monocytogenes in cow milk. J. Dairy Sci. 2016, 99, 1831–1836. [Google Scholar] [CrossRef] [Green Version]
- Braschi, G.; Serrazanetti, D.I.; Siroli, L.; Patrignani, F.; De Angelis, M.; Lanciotti, R. Gene expression responses of Listeria monocytogenes Scott A exposed to sub-lethal concentrations of natural antimicrobials. Int. J. Food Microbiol. 2018, 286, 170–178. [Google Scholar] [CrossRef]
- Upadhyay, A.; Johny, A.K.; Amalaradjou, M.A.R.; Baskaran, S.A.; Kim, K.S.; Venkitanarayanan, K. Plant-derived antimicrobials reduce Listeria monocytogenes virulence factors in vitro, and down-regulate expression of virulence genes. Int. J. Food Microbiol. 2012, 157, 88–94. [Google Scholar] [CrossRef]
- Mith, H.; Duré, R.; Delcenserie, V.; Zhiri, A.; Daube, G.; Clinquart, A. Antimicrobial activities of commercial essential oils and their components against food-borne pathogens and food spoilage bacteria. Food Sci. Nutr. 2014, 2, 403–416. [Google Scholar] [CrossRef] [Green Version]
- Kamdem, S.S.; Belletti, N.; Magnani, R.; Lanciotti, R.; Gardini, F. Effects of carvacrol, (E)-2-hexenal, and citral on the thermal death kinetics of Listeria monocytogenes. J. Food Prot. 2011, 74, 2070–2078. [Google Scholar] [CrossRef]
- Field, D.; Daly, K.; O’Connor, P.M.; Cotter, P.D.; Hill, C.; Ross, R.P. Efficacies of nisin A and nisin V semipurified preparations alone and in combination with plant essential oils for controlling Listeria monocytogenes. Appl. Environ. Microbiol. 2015, 81, 2762–2769. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Veldhuizen, E.J.A.; Creutzberg, T.O.; Burt, S.A.; Haagsman, H.P. Low temperature and binding to food components inhibit the antibacterial activity of carvacrol against Listeria monocytogenes in steak tartare. J. Food Prot. 2007, 70, 2127–2132. [Google Scholar] [CrossRef] [PubMed]
- Niza, E.; Božik, M.; Bravo, I.; Clemente-Casares, P.; Lara-Sanchez, A.; Juan, A.; Klouček, P.; Alonso-Moreno, C. PEI-coated PLA nanoparticles to enhance the antimicrobial activity of carvacrol. Food Chem. 2020, 328, 127131. [Google Scholar] [CrossRef] [PubMed]
- de Sousa, J.P.; de Azerêdo, G.A.; Torres, R.d.A.; Vasconcelos, M.A.d.S.; da Conceição, M.L.; de Souza, E.L. Synergies of carvacrol and 1,8-cineole to inhibit bacteria associated with minimally processed vegetables. Int. J. Food Microbiol. 2012, 154, 145–151. [Google Scholar] [CrossRef]
- Purkait, S.; Bhattacharya, A.; Bag, A.; Chattopadhyay, R.R. Evaluation of antibiofilm efficacy of essential oil components β-caryophyllene, cinnamaldehyde and eugenol alone and in combination against biofilm formation and preformed biofilms of Listeria monocytogenes and Salmonella typhimurium. Lett. Appl. Microbiol. 2020, 71, 195–202. [Google Scholar] [CrossRef]
- 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 2019, 7, 345. [Google Scholar] [CrossRef] [Green Version]
- Apolónio, J.; Faleiro, M.L.; Miguel, M.G.; Neto, L. No induction of antimicrobial resistance in Staphylococcus aureus and Listeria monocytogenes during continuous exposure to eugenol and citral. FEMS Microbiol. Lett. 2014, 354, 92–101. [Google Scholar] [CrossRef] [Green Version]
- Fisher, K.; Phillips, C.A. The effect of lemon, orange and bergamot essential oils and their components on the survival of Campylobacter jejuni, Escherichia coli O157, Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus in vitro and in food systems. J. Appl. Microbiol. 2006, 101, 1232–1240. [Google Scholar] [CrossRef]
- Chen, H.; Zhong, Q. Lactobionic acid enhances the synergistic effect of nisin and thymol against Listeria monocytogenes Scott A in tryptic soy broth and milk. Int. J. Food Microbiol. 2017, 260, 36–41. [Google Scholar] [CrossRef]
- Cusimano, M.G.; Di Stefano, V.; La Giglia, M.; Lo Presti, V.D.M.; Schillaci, D.; Pomilio, F.; Vitale, M. Control of Growth and Persistence of Listeria monocytogenes and β-Lactam-Resistant Escherichia coli by Thymol in Food Processing Settings. Molecules 2020, 25, 383. [Google Scholar] [CrossRef] [Green Version]
- Kerekes, E.-B.; Vidács, A.; Török, J.J.; Gömöri, C.; Petkovits, T.; Chandrasekaran, M.; Kadaikunnan, S.; Alharbi, N.S.; Vágvölgyi, C.; Krisch, J. Anti-listerial effect of selected essential oils and thymol. Acta Biol. Hung. 2016, 67, 333–343. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Penduka, D.; Mosa, R.; Simelane, M.; Basson, A.; Okoh, A.; Opoku, A. Evaluation of the anti-Listeria potentials of some plant-derived triterpenes. Ann. Clin. Microbiol. Antimicrob. 2014, 13, 37. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ferreira, S.; Domingues, F. The antimicrobial action of resveratrol against Listeria monocytogenes in food-based models and its antibiofilm properties. J. Sci. Food Agric. 2016, 96, 4531–4535. [Google Scholar] [CrossRef] [PubMed]
- Yamazaki, K.; Yamamoto, T.; Kawai, Y.; Inoue, N. Enhancement of antilisterial activity of essential oil constituents by nisin and diglycerol fatty acid ester. Food Microbiol. 2004, 21, 283–289. [Google Scholar] [CrossRef]
- Raeisi, M.; Tajik, H.; Rohani, S.M.R.; Tepe, B.; Kiani, H.; Khoshbakht, R.; Aski, H.S.; Tadrisi, H. Inhibitory effect of Zataria multiflora Boiss. essential oil, alone and in combination with monolaurin, on Listeria monocytogenes. Vet. Res. Forum 2016, 7, 7–11. [Google Scholar]
- Miao, X.; Liu, H.; Zheng, Y.; Guo, D.; Shi, C.; Xu, Y.; Xia, X. Inhibitory Effect of Thymoquinone on Listeria monocytogenes ATCC 19115 Biofilm Formation and Virulence Attributes Critical for Human Infection. Front. Cell. Infect. Microbiol. 2019, 9, 304. [Google Scholar] [CrossRef] [Green Version]
- PubChem. Available online: https://pubchem.ncbi.nlm.nih.gov/ (accessed on 14 November 2020).
- Upadhyay, A.; Upadhyaya, I.; Kollanoor-Johny, A.; Venkitanarayanan, K. Antibiofilm effect of plant derived antimicrobials on Listeria monocytogenes. Food Microbiol. 2013, 36, 79–89. [Google Scholar] [CrossRef]
- Cacciatore, F.A.; Dalmás, M.; Maders, C.; Isaía, H.A.; Brandelli, A.; Malheiros, P.d.S. Carvacrol encapsulation into nanostructures: Characterization and antimicrobial activity against foodborne pathogens adhered to stainless steel. Food Res. Int. 2020, 133, 109143. [Google Scholar] [CrossRef]
- Gill, A.O.; Holley, R.A. Mechanisms of bactericidal action of cinnamaldehyde against Listeria monocytogenes and of eugenol against L. monocytogenes and Lactobacillus sakei. Appl. Environ. Microbiol. 2004, 70, 5750–5755. [Google Scholar] [CrossRef] [Green Version]
- Buchrieser, C.; Rusniok, C.; Kunst, F.; Cossart, P.; Glaser, P. Listeria Consortium Comparison of the genome sequences of Listeria monocytogenes and Listeria innocua: Clues for evolution and pathogenicity. FEMS Immunol. Med. Microbiol. 2003, 35, 207–213. [Google Scholar] [CrossRef] [Green Version]
- Milillo, S.R.; Friedly, E.C.; Saldivar, J.C.; Muthaiyan, A.; O’Bryan, C.; Crandall, P.G.; Johnson, M.G.; Ricke, S.C. A review of the ecology, genomics, and stress response of Listeria innocua and Listeria monocytogenes. Crit. Rev. Food Sci. Nutr. 2012, 52, 712–725. [Google Scholar] [CrossRef] [PubMed]
- Silva-Angulo, A.B.; Zanini, S.F.; Rosenthal, A.; Rodrigo, D.; Klein, G.; Martínez, A. Comparative study of the effects of citral on the growth and injury of Listeria innocua and Listeria monocytogenes cells. PLoS ONE 2015, 10, e0114026. [Google Scholar] [CrossRef] [Green Version]
- Gill, A.O.; Holley, R.A. Inhibition of membrane bound ATPases of Escherichia coli and Listeria monocytogenes by plant oil aromatics. Int. J. Food Microbiol. 2006, 111, 170–174. [Google Scholar] [CrossRef] [PubMed]
- Gill, A.O.; Holley, R.A. Disruption of Escherichia coli, Listeria monocytogenes and Lactobacillus sakei cellular membranes by plant oil aromatics. Int. J. Food Microbiol. 2006, 108, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Trinh, N.-T.-T.; Dumas, E.; Thanh, M.L.; Degraeve, P.; Ben Amara, C.; Gharsallaoui, A.; Oulahal, N. Effect of a Vietnamese Cinnamomum cassia essential oil and its major component trans-cinnamaldehyde on the cell viability, membrane integrity, membrane fluidity, and proton motive force of Listeria innocua. Can. J. Microbiol. 2015, 61, 263–271. [Google Scholar] [CrossRef]
- Wang, Y.; Li, X.; Lu, Y.; Wang, J.; Suo, B. Synergistic effect of cinnamaldehyde on the thermal inactivation of Listeria monocytogenes in ground pork. Food Sci. Technol. Int. 2020, 26, 28–37. [Google Scholar] [CrossRef]
- Braschi, G.; Patrignani, F.; Siroli, L.; Lanciotti, R.; Schlueter, O.; Froehling, A. Flow Cytometric Assessment of the Morphological and Physiological Changes of Listeria monocytogenes and Escherichia coli in Response to Natural Antimicrobial Exposure. Front. Microbiol. 2018, 9, 2783. [Google Scholar] [CrossRef] [Green Version]
- Siroli, L.; Patrignani, F.; Gardini, F.; Lanciotti, R. Effects of sub-lethal concentrations of thyme and oregano essential oils, carvacrol, thymol, citral and trans-2-hexenal on membrane fatty acid composition and volatile molecule profile of Listeria monocytogenes, Escherichia coli and Salmonella enteritidis. Food Chem. 2015, 182, 185–192. [Google Scholar] [CrossRef]
- Rogiers, G.; Kebede, B.T.; Van Loey, A.; Michiels, C.W. Membrane fatty acid composition as a determinant of Listeria monocytogenes sensitivity to trans-cinnamaldehyde. Res. Microbiol. 2017, 168, 536–546. [Google Scholar] [CrossRef]
- Karatzas, A.K.; Kets, E.P.; Smid, E.J.; Bennik, M.H. The combined action of carvacrol and high hydrostatic pressure on Listeria monocytogenes Scott A. J. Appl. Microbiol. 2001, 90, 463–469. [Google Scholar] [CrossRef]
- Upadhyay, A.; Upadhyaya, I.; Mooyottu, S.; Venkitanarayanan, K. Eugenol in combination with lactic acid bacteria attenuates Listeria monocytogenes virulence in vitro and in invertebrate model Galleria mellonella. J. Med. Microbiol. 2016, 65, 443–455. [Google Scholar] [CrossRef] [PubMed]
- Lanciotti, R.; Braschi, G.; Patrignani, F.; Gobbetti, M.; De Angelis, M. How Listeria monocytogenes Shapes Its Proteome in Response to Natural Antimicrobial Compounds. Front. Microbiol. 2019, 10, 437. [Google Scholar] [CrossRef] [PubMed]
- Özogul, F.; Kaçar, Ç.; Kuley, E. The Impact of Carvacrol on Ammonia and Biogenic Amine Production by Common Foodborne Pathogens. J. Food Sci. 2015, 80, M2899–M2903. [Google Scholar] [CrossRef] [PubMed]
- Upadhyay, A.; Venkitanarayanan, K. In vivo efficacy of trans-cinnamaldehyde, carvacrol, and thymol in attenuating Listeria monocytogenes infection in a Galleria mellonella model. J. Nat. Med. 2016, 70, 667–672. [Google Scholar] [CrossRef] [PubMed]
- Silva, A.; Genovés, S.; Martorell, P.; Zanini, S.F.; Rodrigo, D.; Martinez, A. Sublethal injury and virulence changes in Listeria monocytogenes and Listeria innocua treated with antimicrobials carvacrol and citral. Food Microbiol. 2015, 50, 5–11. [Google Scholar] [CrossRef]
- Chuang, S.; Sheen, S.; Sommers, C.H.; Zhou, S.; Sheen, L.-Y. Survival Evaluation of Salmonella and Listeria monocytogenes on Selective and Nonselective Media in Ground Chicken Meat Subjected to High Hydrostatic Pressure and Carvacrol. J. Food Prot. 2020, 83, 37–44. [Google Scholar] [CrossRef]
- Moon, H.; Kim, N.H.; Kim, S.H.; Kim, Y.; Ryu, J.H.; Rhee, M.S. Teriyaki sauce with carvacrol or thymol effectively controls Escherichia coli O157:H7, Listeria monocytogenes, Salmonella Typhimurium, and indigenous flora in marinated beef and marinade. Meat Sci. 2017, 129, 147–152. [Google Scholar] [CrossRef]
- Desai, M.A.; Soni, K.A.; Nannapaneni, R.; Schilling, M.W.; Silva, J.L. Reduction of Listeria monocytogenes in raw catfish fillets by essential oils and phenolic constituent carvacrol. J. Food Sci. 2012, 77, M516–M522. [Google Scholar] [CrossRef]
- Moon, H.; Rhee, M.S. Synergism between carvacrol or thymol increases the antimicrobial efficacy of soy sauce with no sensory impact. Int. J. Food Microbiol. 2016, 217, 35–41. [Google Scholar] [CrossRef]
- Upadhyay, A.; Upadhyaya, I.; Kollanoor-Johny, A.; Baskaran, S.A.; Mooyottu, S.; Karumathil, D.; Venkitanarayanan, K. Inactivation of Listeria monocytogenes on frankfurters by plant-derived antimicrobials alone or in combination with hydrogen peroxide. Int. J. Food Microbiol. 2013, 163, 114–118. [Google Scholar] [CrossRef]
- Zhao, Y.; Teixeira, J.S.; Saldaña, M.D.A.; Gänzle, M.G. Antimicrobial activity of bioactive starch packaging films against Listeria monocytogenes and reconstituted meat microbiota on ham. Int. J. Food Microbiol. 2019, 305, 108253. [Google Scholar] [CrossRef] [PubMed]
- Lim, G.O.; Hong, Y.H.; Song, K.B. Application of Gelidium corneum edible films containing carvacrol for ham packages. J. Food Sci. 2010, 75, C90–C93. [Google Scholar] [CrossRef] [PubMed]
- Ravishankar, S.; Jaroni, D.; Zhu, L.; Olsen, C.; McHugh, T.; Friedman, M. Inactivation of Listeria monocytogenes on ham and bologna using pectin-based apple, carrot, and hibiscus edible films containing carvacrol and cinnamaldehyde. J. Food Sci. 2012, 77, M377–M382. [Google Scholar] [CrossRef] [PubMed]
- Ma, Q.; Davidson, P.M.; Zhong, Q. Nanoemulsions of thymol and eugenol co-emulsified by lauric arginate and lecithin. Food Chem. 2016, 206, 167–173. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiao, D.; Davidson, P.M.; Zhong, Q. Spray-dried zein capsules with coencapsulated nisin and thymol as antimicrobial delivery system for enhanced antilisterial properties. J. Agric. Food Chem. 2011, 59, 7393–7404. [Google Scholar] [CrossRef]
- Gadotti, C.; Nelson, L.; Diez-Gonzalez, F. Inhibitory effect of combinations of caprylic acid and nisin on Listeria monocytogenes in queso fresco. Food Microbiol. 2014, 39, 1–6. [Google Scholar] [CrossRef]
- Molinos, A.C.; Abriouel, H.; López, R.L.; Omar, N.B.; Valdivia, E.; Gálvez, A. Enhanced bactericidal activity of enterocin AS-48 in combination with essential oils, natural bioactive compounds and chemical preservatives against Listeria monocytogenes in ready-to-eat salad. Food Chem. Toxicol. 2009, 47, 2216–2223. [Google Scholar] [CrossRef]
- Upadhyay, A.; Upadhyaya, I.; Mooyottu, S.; Kollanoor-Johny, A.; Venkitanarayanan, K. Efficacy of plant-derived compounds combined with hydrogen peroxide as antimicrobial wash and coating treatment for reducing Listeria monocytogenes on cantaloupes. Food Microbiol. 2014, 44, 47–53. [Google Scholar] [CrossRef]
- Zhang, L.; Huang, C.; Xu, Y.; Huang, H.; Zhao, H.; Wang, J.; Wang, S. Synthesis and characterization of antibacterial polylactic acid film incorporated with cinnamaldehyde inclusions for fruit packaging. Int. J. Biol. Macromol. 2020, 164, 4547–4555. [Google Scholar] [CrossRef]
- Gaysinsky, S.; Davidson, P.M.; Bruce, B.D.; Weiss, J. Growth inhibition of Escherichia coli O157:H7 and Listeria monocytogenes by carvacrol and eugenol encapsulated in surfactant micelles. J. Food Prot. 2005, 68, 2559–2566. [Google Scholar] [CrossRef]
- Requena, R.; Vargas, M.; Chiralt, A. Eugenol and carvacrol migration from PHBV films and antibacterial action in different food matrices. Food Chem. 2019, 277, 38–45. [Google Scholar] [CrossRef] [PubMed]
- García-García, R.; López-Malo, A.; Palou, E. Bactericidal action of binary and ternary mixtures of carvacrol, thymol, and eugenol against Listeria innocua. J. Food Sci. 2011, 76, M95–M100. [Google Scholar] [CrossRef] [PubMed]
- De Oliveira, T.L.C.; Leite, B.R.d.C., Jr.; Ramos, A.L.S.; Ramos, E.M.; Piccoli, R.H.; Cristianini, M. Phenolic carvacrol as a natural additive to improve the preservative effects of high pressure processing of low-sodium sliced vacuum-packed turkey breast ham. LWT 2015, 64, 1297–1308. [Google Scholar] [CrossRef]
- Blázquez, I.O.; Burgos, M.J.G.; Pérez-Pulido, R.; Gálvez, A.; Lucas, R. Treatment with High-Hydrostatic Pressure, Activated Film Packaging with Thymol Plus Enterocin AS-48, and Its Combination Modify the Bacterial Communities of Refrigerated Sea Bream (Sparus aurata) Fillets. Front. Microbiol. 2018, 9, 314. [Google Scholar] [CrossRef] [PubMed]
- Leistner, L. Basic aspects of food preservation by hurdle technology. Int. J. Food. Microbiol. 2000, 55, 181–186. [Google Scholar] [CrossRef]
- Singh, S.; Shalini, R. Effect of Hurdle Technology in Food Preservation: A Review. Crit. Rev. Food Sci. Nutr. 2016, 56, 641–649. [Google Scholar] [CrossRef] [PubMed]
- Chung, D.; Cho, T.J.; Rhee, M.S. Citrus fruit extracts with carvacrol and thymol eliminated 7-log acid-adapted Escherichia coli O157:H7, Salmonella typhimurium, and Listeria monocytogenes: A potential of effective natural antibacterial agents. Food Res. Int. 2018, 107, 578–588. [Google Scholar] [CrossRef] [PubMed]
- Guarda, A.; Rubilar, J.F.; Miltz, J.; Galotto, M.J. The antimicrobial activity of microencapsulated thymol and carvacrol. Int. J. Food Microbiol. 2011, 146, 144–150. [Google Scholar] [CrossRef]
- Guevara, L.; Antolinos, V.; Palop, A.; Periago, P.M. Impact of Moderate Heat, Carvacrol, and Thymol Treatments on the Viability, Injury, and Stress Response of Listeria monocytogenes. Biomed Res. Int. 2015, 2015, 548930. [Google Scholar] [CrossRef] [Green Version]
- Ettayebi, K.; El Yamani, J.; Rossi-Hassani, B. Synergistic effects of nisin and thymol on antimicrobial activities in Listeria monocytogenes and Bacillus subtilis. FEMS Microbiol. Lett. 2000, 183, 191–195. [Google Scholar] [CrossRef]
- Olasupo, N.A.; Fitzgerald, D.J.; Narbad, A.; Gasson, M.J. Inhibition of Bacillus subtilis and Listeria innocua by nisin in combination with some naturally occurring organic compounds. J. Food Prot. 2004, 67, 596–600. [Google Scholar] [CrossRef] [PubMed]
- Ait-Ouazzou, A.; Espina, L.; Gelaw, T.K.; de Lamo-Castellví, S.; Pagán, R.; García-Gonzalo, D. New insights in mechanisms of bacterial inactivation by carvacrol. J. Appl. Microbiol. 2013, 114, 173–185. [Google Scholar] [CrossRef] [PubMed]
- Kurek, A.; Nadkowska, P.; Pliszka, S.; Wolska, K.I. Modulation of antibiotic resistance in bacterial pathogens by oleanolic acid and ursolic acid. Phytomedicine 2012, 19, 515–519. [Google Scholar] [CrossRef]
- Zanini, S.F.; Silva-Angulo, A.B.; Rosenthal, A.; Rodrigo, D.; Martínez, A. Effect of citral and carvacrol on the susceptibility of Listeria monocytogenes and Listeria innocua to antibiotics. Lett. Appl. Microbiol. 2014, 58, 486–492. [Google Scholar] [CrossRef] [PubMed]
- Zanini, S.F.; Silva-Angulo, A.B.; Rosenthal, A.; Aliaga, D.R.; Martínez, A. Influence of the treatment of Listeria monocytogenes and Salmonella enterica serovar Typhimurium with citral on the efficacy of various antibiotics. Foodborne Pathog. Dis. 2014, 11, 265–271. [Google Scholar] [CrossRef]
- Santiesteban-López, A.; Palou, E.; López-Malo, A. Susceptibility of food-borne bacteria to binary combinations of antimicrobials at selected aw and pH. J. Appl. Microbiol. 2007, 102, 486–497. [Google Scholar] [CrossRef]
- Sarkar, P.; Bhunia, A.K.; Yao, Y. Impact of starch-based emulsions on the antibacterial efficacies of nisin and thymol in cantaloupe juice. Food Chem. 2017, 217, 155–162. [Google Scholar] [CrossRef] [Green Version]
- Pérez-Conesa, D.; Cao, J.; Chen, L.; McLandsborough, L.; Weiss, J. Inactivation of Listeria monocytogenes and Escherichia coli O157:H7 biofilms by micelle-encapsulated eugenol and carvacrol. J. Food Prot. 2011, 74, 55–62. [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]
- Prakash, A.; Vadivel, V. Citral and linalool nanoemulsions: Impact of synergism and ripening inhibitors on the stability and antibacterial activity against Listeria monocytogenes. J. Food Sci. Technol. 2020, 57, 1495–1504. [Google Scholar] [CrossRef]
- Nostro, A.; Scaffaro, R.; D’Arrigo, M.; Botta, L.; Filocamo, A.; Marino, A.; Bisignano, 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]
- Martínez-Sanz, M.; Bilbao-Sainz, C.; Du, W.-X.; Chiou, B.-S.; Williams, T.G.; Wood, D.F.; Imam, S.H.; Orts, W.J.; Lopez-Rubio, A.; Lagaron, J.M. Antimicrobial Poly(lactic acid)-Based Nanofibres Developed by Solution Blow Spinning. J. Nanosci. Nanotechnol. 2015, 15, 616–627. [Google Scholar] [CrossRef] [PubMed]
- Liu, F.; Saricaoglu, F.T.; Avena-Bustillos, R.J.; Bridges, D.F.; Takeoka, G.R.; Wu, V.C.H.; Chiou, B.-S.; Wood, D.F.; McHugh, T.H.; Zhong, F. Antimicrobial Carvacrol in Solution Blow-Spun Fish-Skin Gelatin Nanofibers. J. Food Sci. 2018, 83, 984–991. [Google Scholar] [CrossRef] [PubMed]
- Liu, F.; Saricaoglu, F.T.; Avena-Bustillos, R.J.; Bridges, D.F.; Takeoka, G.R.; Wu, V.C.H.; Chiou, B.-S.; Wood, D.F.; McHugh, T.H.; Zhong, F. Preparation of Fish Skin Gelatin-Based Nanofibers Incorporating Cinnamaldehyde by Solution Blow Spinning. Int. J. Mol. Sci. 2018, 19, 618. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fonseca, L.M.; Cruxen, C.E.D.S.; Bruni, G.P.; Fiorentini, Â.M.; Zavareze, E.d.R.; Lim, L.-T.; Dias, A.R.G. Development of antimicrobial and antioxidant electrospun soluble potato starch nanofibers loaded with carvacrol. Int. J. Biol. Macromol. 2019, 139, 1182–1190. [Google Scholar] [CrossRef] [PubMed]
- Maftoonazad, N.; Shahamirian, M.; John, D.; Ramaswamy, H. Development and evaluation of antibacterial electrospun pea protein isolate-polyvinyl alcohol nanocomposite mats incorporated with cinnamaldehyde. Mater. Sci. Eng. C 2019, 94, 393–402. [Google Scholar] [CrossRef]
- Knowles, J.; Roller, S. Efficacy of chitosan, carvacrol, and a hydrogen peroxide-based biocide against foodborne microorganisms in suspension and adhered to stainless steel. J. Food Prot. 2001, 64, 1542–1548. [Google Scholar] [CrossRef]
- Wang, Z.; Bai, H.; Lu, C.; Hou, C.; Qiu, Y.; Zhang, P.; Duan, J.; Mu, H. Light controllable chitosan micelles with ROS generation and essential oil release for the treatment of bacterial biofilm. Carbohydr. Polym. 2019, 205, 533–539. [Google Scholar] [CrossRef]
- Cappelier, J.M.; Besnard, V.; Roche, S.; Garrec, N.; Zundel, E.; Velge, P.; Federighi, M. Avirulence of viable but non-culturable Listeria monocytogenes cells demonstrated by in vitro and in vivo models. Vet. Res. 2005, 36, 589–599. [Google Scholar] [CrossRef] [Green Version]
- Lindbäck, T.; Rottenberg, M.E.; Roche, S.M.; Rørvik, L.M. The ability to enter into an avirulent viable but non-culturable (VBNC) form is widespread among Listeria monocytogenes isolates from salmon, patients and environment. Vet. Res. 2010, 41, 8. [Google Scholar] [CrossRef] [Green Version]
- Highmore, C.J.; Warner, J.C.; Rothwell, S.D.; Wilks, S.A.; Keevil, C.W. Viable-but-Nonculturable Listeria monocytogenes and Salmonella enterica Serovar Thompson Induced by Chlorine Stress Remain Infectious. mBio 2018, 9, e00540-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Plant Source (Latin Name) | Plant Source (Common Name) | Compound | Concentration in the EO (%) | References |
---|---|---|---|---|
Thymus vulgaris, Origanum vulgare | thyme, oregano | carvacrol | 2–11 trace–80 | [13,22] |
Anethum graveolens L. | dill seed | carvone S | 45.5 | [22,46] |
Cinnamomum zeylandicum | cinnamon | cinnamaldehyde trans-cinnamaldehyde | 65 | [13,22] |
Cymbopogon citratus | lemongrass | citral | 65–85 | [22,47] |
Eugenia caryophyllata (Syzigium aromaticum L. Myrtaceae) | clove | eugenol | 88.6 | [48] |
Lavandula angustifolia | lavender | linalool | 5–57 | [49] |
Thymus vulgaris, Origanum vulgare | thyme, oregano | thymol | 10–64, trace–64 | [22] |
Psidium guajava L. | guava fruits | (E)-2-hexenal | 7.4 | [50] |
Compound | BA50 Approximate Range (μg/mL) 2 | BA50 as Defined in References (%) 3 |
---|---|---|
thymol | 70 | 0.007 |
cinnamaldehyde | 80–190 | 0.008–0.019 |
4-hydroxytyrosol 4 | 260 | 0.026 |
eugenol | 610–810 | 0.061–0.081 |
carvacrol | 830–860 | 0.083–0.086 |
citral | 990–2000 | 0.099–0.20 |
carvone S | 1700–3500 | 0.17–0.35 |
limonene | 2500 (–>6700) | 0.25 (–>0.67) |
geraniol | 2800–5100 | 0.28–0.51 |
perillaldehyde | 3000–3500 | 0.30–0.35 |
estragole | 3500–3600 | 0.35–0.36 |
benzaldehyde | 3600–4600 | 0.36–0.46 |
salicylaldehyde | 4300–4500 | 0.43–0.45 |
cironella S | 4400–7000 | 0.44–0.70 |
cironella R | 4500–12,000 | 0.45–1.2 |
menthol | 4800–5700 | 0.48–0.57 |
Compound | MIC Approximate Range 1 (μg/mL) | MIC as Defined in References 2 | Strains(s) Used in the Reference Study | References |
---|---|---|---|---|
carvacrol | 65 | 65 μg/mL | ATCC 15313 | [57] |
100 | 100 mg/L | Scott A | [58] | |
113 | 0.75 mM | ATCC 19115, Scott A, Presque-598 | [59] | |
125 | 0.125 μL/mL | NCTC 11994, S0580 | [60] | |
125–300 | 125–300 mg/L 3 | 56LY | [61] | |
156–625 | 156–625 μg/mL | EGDe, LO28, F2356, 33413, 33013 | [62] | |
245 | 1.63 mM | Isolate was not defined 4 | [63] | |
256–>1024 | 256–>1024 μg/mL 5 | ATCC 7644 | [64] | |
600 | 0.6 μL/mL | ATCC 7644 | [65] | |
cinnamaldehyde | 65 | 65 μg/mL | ATCC 15313 | [57] |
83 | 83.33 μg/mL | MTCC 657 | [66] | |
500–1000 | 500–1000 ppm | ATCC 15313, H7962, NADC 2045 (Scott A) | [41] | |
512 | 512 μg/mL | CMCC 54004 | [53] | |
trans-cinnamaldehyde | 119 | 0.90 mM | ATCC 19115, Scott A, Presque-598 | [59] |
125–250 | 0.125–0.25 μL/mL | NCTC 11994, S0580 | [60] | |
156–312 | 156–312 μg/mL | EGDe, LO28, F2356, 33413, 33013 | [62] | |
250 | 0.25 mg/mL | SZMC 21307 | [67] | |
citral | 60–80 80–100 | 0.06–0.08 mg/mL 0.08–0.1 mg/mL 6 | EGD, Scott A, C882 | [68] |
225–400 | 225–400 mg/L 3 | 56LY | [61] | |
250 | 250 mg/L | Scott A | [58] | |
300 | 0.03% v/v | ATCC 7644 (C3970) | [69] | |
eugenol | 67 | 66.66 μg/mL | MTCC 657 | [66] |
80 | 0.08 mg/mL | EGD, Scott A, C882 | [68] | |
90 | 90 μg/mL | ATCC 15313 | [57] | |
500 | 0.5 μL/mL | NCTC 11994, S0580 | [60] | |
1024 | 1024 μg/mL | CMCC 54004 | [53] | |
linalool | 750–1000 | 0.75–1 μL/mL | NCTC 11994, S0580 | [60] |
2500 | 0.25% v/v | ATCC 7644 (C3970) | [69] | |
thymol | 90 | 0.60 mM | ATCC 19115, Scott A, Presque-598 | [59] |
150 | 150 μg/mL | ATCC 15313 | [57] | |
156–312 | 156–312 μg/mL | EGDe, LO28, F2356, 33413, 33013 | [62] | |
250 | 0.25 mg/mL | Scott A | [70] | |
250–800 | 250–800 μg/mL | ATCC 7644, ATCC 19114, ATCC 19115, NCTC 10887, NCTC 18890 and 25 strains from different foods 7 | [71] | |
250 | 0.25 μL/mL | NCTC 11994, S0580 | [60] | |
500 | 0.5 mg/mL | SZMC 21307 | [72] | |
1024 | 1024 μg/mL | CMCC 54004 | [53] | |
(E)-2-hexenal | 325–1400 | 325–1400 mg/L 3 | 56LY | [61] |
800 | 800 mg/L | Scott A | [58] | |
1,8-cineole | 20,000 | 20 μL/mL | ATCC 7644 | [65] |
β-caryophyllene | 167 | 166.66 μg/mL | MTCC 657 | [66] |
3β-acetylursolic acid | 1670 | 1.67 mg/mL | ATCC 19115 | [73] |
methyl-3β-hydroxylanosta-9,24-dienoate | 185 | 0.185 mg/mL | ATCC 19115 | [73] |
3β-hydroxylanosta-9,24-dien-21-oic acid | 185 | 0.185 mg/mL | ATCC 19115 | [73] |
resveratrol | 200 | 200 mg/L | LMG 16779, LMG 16780, LMG 13305 | [74] |
diglicerol monolaurate | 50 | 0.005% | IID 581 | [75] |
monolaurin | 31–125 | 31.25–125 μg/mL 8 | ATCC 19118 | [76] |
terpinene-4-ol | 4000 | 4 mg/mL | SZMC 21307 | [67] |
thymoquinone | 6–13 | 6.25–12.50 μg/mL | ATCC 19115, ATCC 15313 and 6 strains from different foods 9 | [77] |
berberine | 8192 | 8192 μg/mL | CMCC 54004 | [53] |
Compound | MBC, Approximate Range 1 (μg/mL) | MBC as Defined in References 2 | Strains(s) Used in the Study | References |
---|---|---|---|---|
carvacrol | 150–300 | 150–300 mg/L 3 | 56LY | [61] |
250 | 0.25 μL/mL | NCTC 11994, S0580 | [60] | |
255 | 1.7 mmol/L | IID 581 | [75] | |
751 | 5.0 mM | ATCC 19115, Scott A, Presque-598 | [79] | |
1770 | 1.77 mg/mL | MBC was determined for bacterial pool of strains: ATCC 7644, 7459 and J11 | [80] | |
cinnamaldehyde | 92 | 91.66 μg/mL | MTCC 657 | [66] |
1004 | 7.6 mmol/L | IID 581 | [75] | |
3965 | 30 mM | CRIFS C717 | [81] | |
trans-cinnamaldehyde | 500 | 0.5 μL/mL | NCTC 11994, S0580 | [60] |
661 | 5.0 mM | ATCC 19115, Scott A, Presque-598 | [79] | |
citral | 80–100 | 0.08–0.1 mg/mL | EGD, Scott A, C882 | [68] |
250–450 | 250–450 mg/L 3 | 56LY | [61] | |
eugenol | 67 | 66.66 μg/mL | MTCC 657 | [66] |
100 | 0.1 mg/mL | EGD, Scott A, C882 | [68] | |
821 | 5 mM | CRIFS C717 | [81] | |
1000 | 1 μL/mL | NCTC 11994, S0580 | [60] | |
1002 | 6.1 mmol/L | IID 581 | [75] | |
3087 | 18.5 mM | ATCC 19115, Scott A, Presque-598 | [79] | |
isoeugenol | 1248 | 7.6 mmol/L | IID 581 | [75] |
thymol | 496 | 3.3 mmol/L | IID 581 | [75] |
496 | 3.3 mM | ATCC 19115, Scott A, Presque-598 | [79] | |
500 | 0.5 μL/mL | NCTC 11994, S0580 | [60] | |
500 | 0.5 mg/mL | Scott A | [70] | |
(E)-2-hexenal | 325–1400 | 325–1400 mg/L 3 | 56LY | [61] |
diglycerol monocaprinate | 200 | 0.02% | IID 581 | [75] |
diglicerol monolaurate | 100 | 0.01% | IID 581 | [75] |
diglycerol monomyristate | 200 | 0.02% | IID 581 | [75] |
Row | Food Category | Food Product Description | Approx. Initial Contamination 1 | Storage Time and Temp. | Treatment(s) That Resulted in the Most Significant Pathogen Reduction 2 | Approx. Final Contamination 1 | Ref. | |
---|---|---|---|---|---|---|---|---|
In Food Product | In Control Sample | |||||||
AA | Meat | Fresh ground chicken meat (ca. 98% lean, 2% fat, without additives) | 107 to 108 CFU/g | 3 days 10 °C | 0.75% (w/w) carvacrol | 6.27 log CFU/g | 7.94 log CFU/g | [98] |
AB | Meat | Fresh ground chicken meat (ca. 98% lean, 2% fat, without additives) | 107 to 108 CFU/g | 7 days 4 °C | 0.75% (w/w) carvacrol + 300 MPa OR 0.60% or 0.75% (w/w) carvacrol + 350 MPa | n.d. 3 (<1 log CFU/g) | 7 log CFU/g (in S 4 treated with HPP only) | [98] |
AC | Meat | Fresh ground chicken meat (ca. 98% lean, 2% fat, without additives) | 107 to 108 CFU/g | 7 days 10 °C | 0.60% or 0.75% (w/w) carvacrol + 350 MPa | n.d. (<1 log CFU/g) | 8 log CFU/g (in S treated with HPP only) | [98] |
AD | Meat | Fresh, skinless chicken breast fillets | 102 CFU/cm2 before 24 h bacterial pregrowth | 48 h 6 °C | 0.25 mg/mL thymol + 5% (w/v) salt 5 | 2.2 log CFU/cm2 (non-washed S); 3.0 log CFU/cm2 (washed S) | 4.9 log CFU/cm2 (non-washed S); 3.9 log CFU/cm2 (washed S) | [72] |
AE | Meat | Beef sirloins | 3.3 log CFU/g | 7 d 4 °C | 0.5% thymol 5 | n.d. | 3.4 log CFU/g (not marinated S); 2.7 log CFU/g (S marinated in teriyaki sauce) | [99] |
AF | Meat | Raw pork loin | 105 CFU/g | 12 h 4 °C | 15 ppm carvacrol + 6 ppm grapefruit seed extract + 4.5 ppm nisin 5 | 2.88 log reduction achieved | N/A 6 | [41] |
AG | Meat | Steak tartare (ground beef mixed with Filet Américain sauce) | 107 CFU/g | 4 weeks 10 °C | 5 mmole/g carvacrol | 108 CFU/g | 108 CFU/g | [63] |
AH | Skin | Heat sterilized chicken skin | 8.0 log CFU/sample | N/A | 0.25% (v/v) linalool 5 | 6.2 log CFU/sample | not presented | [69] |
AI | Fish | Channel catfish fillets | 3.9 log CFU/g | 10 d 4 °C | 2% carvacrol 5 | n.d. (<1.3 log CFU/mL) | 5.5 log CFU/g | [100] |
AJ | Marinating solution | Marinade containing 5% (w/v) salt and thymol; control sample contained salt only | N/A (3.3 log CFU/cm2 in control Ss after 24 h) | 48 h 6 °C | 0.25 mg/mL thymol + 5% (w/v) salt 5 | 2.1 log CFU/cm2 | 4.0–5.0 log CFU/cm2 | [72] |
AK | Meat juice | Centrifuged and filtered chicken juice from defrosted commercially frozen chickens without viscera | 6.5 log CFU/mL | 14 d 4 °C | 400 mg/L resveratrol OR 200 mg/L resveratrol | 6 log CFU/mL | 8.5 log CFU/mL | [74] |
AL. | Soy sauce | Commercially available preservative-free soy sauce | 7.3 log CFU/mL | 14 d 22 °C or 4 °C | 1 mM carvacrol OR 1 mM thymol | n.d. | 0 log CFU/mL reduction achieved | [101] |
AM | Teriyaki sauce | Commercially available sauce (soy sauce, wine, high fructose corn syrup, water, vinegar, salt, spices, onion powder, and garlic powder) | 0 log CFU/mL | 7 d 4 °C | 0.3% or 0.5% carvacrol OR 0.3% or 0.5% thymol | n.d. | 3.1 log CFU/mL | [99] |
AN | Meat product | Fresh, skinless, pork–beef frankfurters (20% fat) | 6 log CFU/frankfurter | 70 d 4 °C | 0.75% trans-cinnamaldehyde + 0.1% hydrogen peroxide 5 | n.d. | 7.3 log CFU/frankfurter | [102] |
AO | Meat product | Fresh, skinless, pork–beef frankfurters (20% fat) | 6 log CFU/frankfurter | 70 d 4 °C | 0.75% trans-cinnamaldehyde + 0.1% hydrogen peroxide OR 0.75% carvacrol + 0.1% hydrogen peroxide 5 | n.d. | 6 log CFU/frankfurter | [102] |
AP | Meat product | Cooked ham with 3% (w/w) sodium chloride | 2.5 log CFU/cm2 | 28 d 4 °C | 0.195 g carvacrol + 0.025 g chitosan OR 0.1 g gallic acid+ 0.15 g chitosan (amounts of per 1 g of starch in film) | n.d. (<100 CFU/cm2) | 9 log CFU/cm2 | [103] |
AQ | Meat product | Ham | 7.3 log CFU/g | 9 d 4 °C | 0.6% carvacrol (concentration in film) | 4.5 log CFU/g | 6.1 log CFU/g | [104] |
AR | Meat product | Cooked ham | 5.0 log CFU/g | 7 d 4 °C | 3% carvacrol (in apple or hibiscus or carrot film) | n.d. (<1.3 log CFU/g) | 4.4–4.6 log CFU/g (depending on the type of film) | [105] |
AS | Meat product | Bologna | 5.0 log CFU/g | 7 d 4 °C | 3% carvacrol in hibiscus film OR 3% carvacrol in apple film (OR 1.5% carvacrol in hibiscus film) | 2.25 log CFU/g (3.0 log CFU/g) | 4.5–4.8 log CFU/g (depending on the type of film) | [105] |
AT | Milk | Pasteurized cow milk type A; 3% fat | 6 log CFU/mL | 6 d 4 °C | 37.5 μg/mL thymol + 31.25 μg/mL nisin | 4 log CFU/mL | 6 log CFU/mL | [57] |
AU | Milk | Ultra-high-temperature (UHT) processed 2% reduced-fat milk | 6.5 log CFU/mL | 120 h 21 °C | 2 mg/mL thymol + 500 IU/mL nisin + 10 mg/mL lactobionic acid OR 2 mg/mL thymol + 250 IU/mL nisin + 10 mg/mL lactobionic acid | n.d. (<1 log CFU/mL) | 8.75 CFU/mL | [70] |
AV | Milk | Ultra-high-temperature (UHT) whole milk | 6.5 log CFU/mL | 120 h 21 °C | 2 mg/mL thymol + 500 IU/mL nisin + 10 mg/mL lactobionic acid | 2 log CFU/mL | 8.3 CFU/mL | [70] |
AW | Milk | Ultra-high-temperature (UHT)-treated skim milk | 6.2 log CFU/mL | 14 d 4 °C | 400 mg/L resveratrol | 7.8 log CFU/mL | 8.5 log CFU/mL | [74] |
AX | Milk | Ultra-high-temperature (UHT)-treated whole milk | 6.2 log CFU/mL | 14 d 4 °C | 400 mg/L resveratrol OR 200 mg/L resveratrol | 8.0 log CFU/mL | 8.3 log CFU/mL | [74] |
AY | Milk | Semi-skimmed milk | not presented | N/A | 3 mmol/L carvacrol + 300 MPa HHP | 3.2 log reduction in viable counts achieved | 0.0 log reduction in viable counts achieved | [92] |
AZ | Milk | 2% reduced fat milk | 5.5 log CFU/mL | 120 h 21 °C | 750 ppm of nanoemultions containing 1% of eugenol or thymol and other compounds (see comments in Table 6) | 1.2 log CFU/mL | 8.8 log CFU/mL | [106] |
BA | Milk | 2% reduced fat UHT milk | 6.3 log CFU/mL | 48 h 25 °C | capsules prepared by spray drying nisin extract with 1% w/v thymol (and other compounds—see comments in Table 6); concentration of capsules was adjusted to nisin concentration of 400 IU/mL | 8.1–8.5 log CFU/mL | 9 log CFU/mL | [107] |
BB | Cheese | Queso fresco cheese manufactured by authors | 3.2 log CFU/g–4.3 log CFU/g (depending on bacterial cocktail) | 20 days 4 °C | 0.72 g/kg caprylic acid + 0.49 g/kg nisin | 2.2 log CFU/g–4.4 log CFU/g (depending on bacterial cocktail) | 8.6 log CFU/g–8.2 log CFU/g (depending on bacterial cocktail) | [108] |
BC | Cheese | Queso fresco cheese manufactured by authors | 3.8 log CFU/g | 20 days 4 °C | 0.6 g/kg trans-cinnamaldehyde + 0.36 g/kg caprylic acid + 0.49 g/kg nisin | 3.6 log CFU/g | 7.0 log CFU/g | [108] |
BD | Salad | RTE Russian salad of pH 4.44 (boiled: potatoes, carrots, peas, egg and raw olives, with mayonnaise) | 4.67 log CFU/g | 24 h 10 °C | 5 mM thymol + 20 μg/g enterocin AS-48 OR 30 mM terpineol + 20 μg/g enterocin AS-48 OR 0.5 mM tyrosol + 20 μg/g enterocin AS-48 | n.d. | 4.57 log CFU/g | [109] |
BE | Leafy vegetables | Fresh mix of iceberg lettuce, chard and rocket (in a rate of 1:1:1), hand shredded | not presented | N/A | 0.6 μg/mL carvacrol 5 | n.d. (<2 log CFU/g) | 8.5 log CFU/g | [65] |
BF | Vegetable model | Mix of iceberg lettuce, chard and rocket (60 g of each) mixed with 400 mL of water, blended, filtered and sterilized by filtration | 6.2 log CFU/mL | 24 h 37 °C | 0.6 μg/mL carvacrol OR 20 μg/mL 1,8-cinole OR 0.075 μg/mL carvacrol + 2.5 μg/mL 1,8-cinole OR 0.15 μg/mL carvacrol + 5 μg/mL 1,8-cinole | n.d. (<2 log CFU/g) | 8.2 log CFU/g | [65] |
BG | Vegetable model | Iceberg lettuce (50 g) homogenized with 100 mL of water, adjusted to pH 7.2 by phosphate buffer, then autoclaved | 6.2 log CFU/mL | 14 d 4 °C | 400 mg/L resveratrol OR 200 mg/L resveratrol | 6.2 log CFU/mL | 7.2 log CFU/mL | [74] |
BH | Vegetables | Cabbage leaves (Sweetheart) | 8.0 log CFU/sample | N/A | 0.25% (v/v) linalool 5 | n.d. | not presented | [69] |
BI | Vegetables | Cabbage leaves (Sweetheart) | 8.0 log CFU/sample | 24 h 37 °C | 1.85 mL/L beaker of citral OR 1.85 mL/L beaker of linalool | 2.2 log CFU/sample | not presented | [69] |
BJ | Vegetable | Lettuce leaves | 105 CFU/g | 12 h 4 °C | 15 ppm carvacrol + 6 ppm grapefruit seed extract + 4.5 ppm nisin 5 | 5 log reduction achieved | N/A | [41] |
BK | Fruit | Red delicious apples, sliced | 565 CFU/mL | 10 days 5 °C | 500 μg/mL rosmaric acid 5 | 28 CFU/mL | uncountable | [56] |
BL | Fruit | Cantaloupe rind plugs prepared from fresh, whole cantaloupes, | 7.3 log CFU/cm2 | N/A | 2% caprylic acid (alone or + 2% hydrogen peroxide) OR 2% thymol (alone or + 2% hydrogen peroxide) OR 2% carvacrol + 2% hydrogen peroxide 5 | n.d. | 4.9 log CFU/cm2 | [110] |
BM | Fruit | Cantaloupe rind plugs prepared from fresh, whole cantaloupes, | 7.1 log CFU/cm2 | 7 d 4 °C | 2% caprylic acid (alone or +2% hydrogen peroxide) OR 2% thymol (alone or +2% hydrogen peroxide) OR 2% carvacrol (+2% hydrogen peroxide) 5 | n.d. | 7.3 log CFU/cm2 | [110] |
BN | Juice | Steam-heated filtered carrot juice from fresh, raw Nantesa carrots, that were peeled, washed and minced | N/A (8.2 log CFU/mL in control sample after 24 h) | 24 h 30 °C | 1.6 mmol/L carvacrol + 1.6 mmol/L cymene | 2.5 log CFU/mL | 8.2 log CFU/mL | [52] |
Row | Listeria monocytogenes Strain(s) Used in the Study | Other Treatments Presented in the Study 1 | Comments | Ref. |
---|---|---|---|---|
AA | 4-strain cocktail of: F4243, F4249, ATCC 7644, ATCC 43256 | 0.15%, 0.30%, 0.45% and 0.60% carvacrol | Chicken meat was manually mixed with targeted amount of carvacrol | [98] |
AB | 4-strain cocktail of: F4243, F4249, ATCC 7644, ATCC 43256 | Combinations of 0.15%, 0.30%, 0.45% or 0.60% carvacrol +300 MPa or 350 MPa | Chicken meat was manually mixed with targeted amount of carvacrol | [98] |
AC | 4-strain cocktail of: F4243, F4249, ATCC 7644, ATCC 43256 | Combinations of 0.15%, 0.30%, 0.45% or 0.60% carvacrol +300 MPa or 350 MPa | Chicken meat was manually mixed with targeted amount of carvacrol | [98] |
AD | NCAIM B01934 | N/A 2 | Samples were initially washed with water (or not), inoculated and kept for 24 h at 6 °C, and then marinated in marinates containing 5% (w/v) salt and thymol; control sample contained salt only | [72] |
AE | 3-strain cocktail of: ATCC 19111, 19115, 19117 | 0.3% thymol 0.3% and 0.5% carvacrol 3 | Samples were inoculated, kept overnight at 4 °C and then marinated (or not) in marinates containing teriyaki sauce alone or with carvacrol or thymol | [99] |
AF | 3- strain cocktail of: ATCC 15313, H7962, NADC 2045 (Scott A) | Various combinations of carvacrol (1.6–18 ppm) + grapefruit seed extract (0.64–7.36) + nisin (1.6–18.4) 2 | 90 mL of an antibacterial solution was added to 10 g samples | [41] |
AG | Isolate was not defined, (described as “Dutch field isolate obtained from cheese”) | N/A | Control samples and treated samples were equally contaminated at the end of storage | [63] |
AH | ATCC 7644 (C3970) | 0.03% (v/v) citral 3 | Effects of 60 s subjecting to antimicrobial solutions were measured; samples were not stored after treatment | [69] |
AI | 4-strain cocktail of not defined strains (described as serotypes 1/2b, 3b, 4b, and 4c previously “isolated from catfish processing facilities”) | 1% carvacrol 3 | Inoculated samples were dipped in 30 mL of carvacrol solution for 30 min at 4 °C; after treatment the solutions were drained out | [100] |
AJ | NCAIM B01934 | N/A | Inoculated chicken samples (washed or not prior inoculation) were immersed in the solution | [72] |
AK | LMG 16779 serovar 1/2a | N/A | - | [74] |
AL | 3-strain cocktail of: ATCC 19111, 19115, 19117 | 1 mM eugenol; 1 mM trans-cinnamaldehyde; 1 mM β-resorcylic acid; 1 mM of vanillin | Substances other than carvacrol and thymol were not able to effectively reduce the pathogen during 10 min treatment and were not tested up to 14 days | [101] |
AM | 3-strain cocktail of: ATCC 19111, 19115, 19117 | N/A | Inoculated beef was marinated in the sauce and leftover marinade was stored and examined | [99] |
AN | 5-strain cocktail of: ATCC Scott A, ATCC 19115, 101, 1, Presque-598 | 0.75% trans-cinnamaldehyde; 0.75% carvacrol; 0.75% carvacrol + 0.1% hydrogen peroxide 3 | Frankfurters were immersed in dipping solutions for 60 s and held at 55 °C | [102] |
AO | 5-strain cocktail of ATCC Scott A, ATCC 19115, 101, 1, Presque-598 | 0.75% trans-cinnamaldehyde; 0.75% carvacrol 3 | Frankfurters were immersed in dipping solutions for 30 s and held at 65 °C | [102] |
AP | 5-strain cocktail of: FSL J1-177, FSL C1-056, FSL N3-013, FSL R2-499, FSL N1-227 | or 0.3 g gallic acid 0.3 g gallic acid + 0.025 g chitosan 0.048 g carvacrol + 0.025 g chitosan (amounts of antimicrobial per 1 g of starch in film) | Ham was covered with film made of cull potato starch | [103] |
AQ | KCTC 3710 | 0.4% carvacrol (concentration in film) | Ham was covered with film made of Gelidium corneum | [104] |
AR | strain 101M; serotype 4b | 0.5%, 1.5% and 3% cinnamaldehyde 0.5% and 1.5% carvacrol (concentration in films) | Ham was covered with apple, carrot, or hibiscus films incorporated with carvacrol or cinnamaldehyde | [105] |
AS | strain 101M; serotype 4b | Other combinations of 0.5%, 1.5% or 3% either cinnamaldehyde or carvacrol in all types of films | Bologna was covered with apple, carrot or hibiscus films incorporated with carvacrol or cinnamaldehyde; | [105] |
AT | ATCC 15313 | (37.5 μg/mL thymol or 16.25 μg/mL carvacrol or 22.5 μg/mL eugenol or 16.25 μg/mL cinnamaldehyde) + 31.25 μg/mL nisin | - | [57] |
AU | Scott A | Nisin (up to 500 IU/mL), thymol (up to 10 mg/mL) and lactobionic acid (up to 10 mg/mL) alone or in binary and ternary combinations | - | [70] |
AV | Scott A | Nisin (up to 500 IU/mL), thymol (up to 10 mg/mL) and lactobionic acid (up to 10 mg/mL) alone or in binary and ternary combinations | - | [70] |
AW | LMG 16779 serovar 1/2a | 200 mg/L resveratrol | - | [74] |
AX | LMG 16779 serovar 1/2a | N/A | Differences in final bacterial counts in treated and control samples were not statistically significant | [74] |
AY | Scott A | 3 mmol/L carvacrol; 300 MPa HHP | Effects of 20 min treatment with antimicrobial and HHP (separately or in combination) at 1 °C were measured; samples were not stored after treatment | [92] |
AZ | Scott A | N/A | Nanoemultions were prepared with 1% w/w of thymol or eugenol and 0.93% w/w lauric arginate and 1% w/w lecithin | [106] |
BA | Scott A | N/A | Treatment was done with food-grade capsules prepared by spray drying nisin extract (adjusted to 70% aqueous ethanol) with 2% w/v zein, 1% w/v thymol, and glycerol at concentrations 0.05%, 0.1%, 0.5% or 0% (w/v) | [107] |
BB | 5- or 6-strain cocktails (A): R2-500, N1-227, N3-031, J1-110, J1-119, R2-502, (B): ATCC 15313, H7762, 2349, 3528, 2422, (C): N3-013, J1-158, J1-169, J1-049, C1-056, (D): DUP-1051D, DUP-1039B, 116-1501-S-4, DUP-1039C, DUP-1059A, (E): 116-110-S-2, DUP-1039E, DUP-1052, ATCC 51775, DUP-1042B | 0.36 g/kg caprylic acid + 0.49 g/kg nisin; (0.36 g/kg caprylic acid + 0.40 g/kg nisin − tested with C, D and E cocktails only) | Antimicrobials were added during cheese manufacturing | [108] |
BC | 5-strain cocktail of: DUP-1030A, DUP-1042, DUP-1042C, DUP-1052A, DUP-10142 | 0.3, 0.6 or 1.2 g/kg trans-cinnamaldehyde; 0.36 g/kg caprylic acid + 0.49 g/kg nisin; 0.3 g/kg trans-cinnamaldehyde + 0.36 g/kg caprylic acid + 0.49 g/kg nisin | Antimicrobials were added during cheese manufacturing | [108] |
BD | CECT 4032 (serotype 4b, previously isolated from a case of meningitis) | (30 mM carvacrol or 1 mM caffeic acid or 10 mM coumaric acid or 10 mM ferulic acid or 1 mM vanillic acid) +20 μg/g enterocin AS-48 | Antimicrobials were mixed with salad by gently rolling a pipette over a salad bag | [109] |
BE | ATCC 7644 | 20 μg/mL 1,8-cinole; 0.3 μg/mL carvacrool + 10 μg/mL 1,8-cinole; 0.15 μg/mL carvacrool + 5 μg/mL 1,8-cinole 3 | Effects of 5 min treatment (submerging in solutions) with antimicrobials at 28 °C were measured; vegetables were not stored after treatment; | [65] |
BF | ATCC 7644 | N/A | - | [65] |
BG | LMG 16779 serovar 1/2a | N/A | - | [74] |
BH | ATCC 7644 (C3970) | 0.03% (v/v) citral 3 | Effects of 60 s subjecting into antimicrobial solutions were measured; samples were not stored after treatment | [69] |
BI | ATCC 7644 (C3970) | N/A | Samples were not in contact with solutions, but with antimicrobial vapors | [69] |
BJ | 3- strain cocktail of: ATCC 15313, H7962, NADC 2045 (Scott A) | Various combinations of carvacrol (1.6–18 ppm) + grapefruit seed extract (0.64–7.36) + nisin (1.6–18.4) 3 | 90 mL of an antibacterial solution was added to 10 g samples | [41] |
BK | MTCC No. 1143 | 500 μg/mL caffeic acid; 500 μg/mL p-Coumaric acid; 500 μg/mL hydroxyl phenyllactic acid; 500 μg/mL tranc sinnamic acid | Apples were immersed in the solutions and then inoculated by dipping in bacterial suspensions | [56] |
BL | 5-strain cocktail of: Scott A (ATCC), 19115 (ATCC), 101, 1, Presque-598 | 2% carvacrol 3 | Washing treatments were applied to rind plugs at 3 levels of temperature (25–65 °C) and at 3 levels of time (exact values depended on temperature); only 65 °C for 5 min washing results are presented in the table as it was the most effective | [110] |
BM | 5-strain cocktail of Scott A (ATCC), 19115 (ATCC), 101, 1, Presque-598 | N/A | Chitosan-based coating treatment was applied to surface-inoculated cantaloupes | [110] |
BN | STCC4031 | 0.4, 0.8 or 1.2 mmol/L of carvacrol and cymene combined | - | [52] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 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
Kawacka, I.; Olejnik-Schmidt, A.; Schmidt, M.; Sip, A. Natural Plant-Derived Chemical Compounds as Listeria monocytogenes Inhibitors In Vitro and in Food Model Systems. Pathogens 2021, 10, 12. https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10010012
Kawacka I, Olejnik-Schmidt A, Schmidt M, Sip A. Natural Plant-Derived Chemical Compounds as Listeria monocytogenes Inhibitors In Vitro and in Food Model Systems. Pathogens. 2021; 10(1):12. https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10010012
Chicago/Turabian StyleKawacka, Iwona, Agnieszka Olejnik-Schmidt, Marcin Schmidt, and Anna Sip. 2021. "Natural Plant-Derived Chemical Compounds as Listeria monocytogenes Inhibitors In Vitro and in Food Model Systems" Pathogens 10, no. 1: 12. https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10010012