Antimicrobial Effects of Plant Compounds against Virulent Escherichia coli O157:H7 Strains Containing Shiga Toxin Genes in Laboratory Media and on Romaine Lettuce and Spinach
Escherichia coli strains produce Shiga-toxins Stx-1 and Stx-2 that contribute to their
virulence. The objective was to evaluate antimicrobial activities of plant
essential oils (oregano, cinnamon, lemongrass), their active components (carvacrol,
cinnamaldehyde, citral) and plant-extracts (green tea polyphenols, apple skin,
black tea, decaffeinated black tea, grapeseed and pomace extracts) against E. coli O157:H7 strains containing Stx-1 and
References
[1]
Marshall, K.E., Nguyen, T.A., Ablan, M., Nichols, M.C., Robyn, M.P., Sundararaman, P., et al. (2020) Investigations of Possible Multistate Outbreaks of Salmonella, Shiga Toxin-Producing Escherichia coli, and Listeria monocytogenes Infections—United States, 2016. Surveillance Summaries, 69, 1-14.
[2]
Smith, A.M., Tau, N.P., Kalule, B.J., Nicol, M.P., McCulloch, M., Jacobs, C.A., et al. (2019) Shiga Toxin-Producing Escherichia coli O26:H11 Associated with a Cluster of Haemolytic Uraemic Syndrome Cases in South Africa, 2017. Access Microbiology, 1, e000061.
[3]
Rasooly, R., Do, P.M., Levin, C.E. and Friedman, M. (2010) Inhibition of Shiga Toxin 2 (Stx2) in Apple Juices and Its Resistance to Pasteurization. Journal of Food Science, 75, M296-M301. https://doi.org/10.1111/j.1750-3841.2010.01615.x
[4]
Rasooly, R., Do, P.M., Griffey, S.M., Vilches-Moure, J.G. and Friedman, M. (2010) Ingested Shiga Toxin 2 (Stx2) Causes Histopathological Changes in Kidney, Spleen and Thymus Tissues and Mortality in Mice. Journal of Agricultural and Food Chemistry, 58, 9281-9286. https://doi.org/10.1021/jf101744z
[5]
Hussein, H.S. (2007) Prevalence and Pathogenicity of Shiga Toxin-Producing Escherichia coli in Beef Cattle and Their Products. Journal of Animal Science, 85, E63-E72. https://doi.org/10.2527/jas.2006-421
[6]
Kamaruzzaman, E.A., Abdul Aziz, S., Bitrus, A.A., Zakaria, Z. and Hassan, L. (2020) Occurrence and Characteristics of Extended-Spectrum Β-Lactamase-Producing Escherichia coli from Dairy Cattle, Milk, and Farm Environments in Peninsular Malaysia. Pathogens, 9, Article No. 1007. https://doi.org/10.20944/preprints202009.0485.v1
[7]
Ramos, S., Silva, V., Dapkevicius, M.d.L.E., Cania, M., Tejedor-Junco, M.T., Igrejas, G., et al. (2020) Escherichia coli as Commensal and Pathogenic Bacteria among Food-Producing Animals: Health Implications of Extended Spectrum β-Lactamase (Esbl) Production. Animals, 10, Article No. 2239. https://doi.org/10.3390/ani10122239
[8]
Francis, G.A. and O’Beirne, D. (2001) Effects of Vegetable Type, Package Atmosphere and Storage Temperature on Growth and Survival of Escherichia coli O157: H7 and Listeria monocytogenes. Journal of Industrial Microbiology and Biotechnology, 27, 111-116. https://doi.org/10.1038/sj.jim.7000094
[9]
Kiskó, G. and Roller, S. (2005) Carvacrol and P-Cymene Inactivate Escherichia coli O157:H7 in Apple Juice. BMC Microbiology, 5, Article No. 36. https://doi.org/10.1186/1471-2180-5-36
[10]
Kim, J., Marshall, M.R. and Wei, C.-I. (1995) Antibacterial Activity of Some Essential Oil Components against Five Foodborne Pathogens. Journal of Agricultural and Food Chemistry, 43, 2839-2845. https://doi.org/10.1021/jf00059a013
[11]
Dušan, F., Marián, S., Katarína, D. and Dobroslava, B. (2006) Essential Oils-Their Antimicrobial Activity against Escherichia coli and Effect on Intestinal Cell Viability. Toxicology in Vitro, 20, 1435-1445. https://doi.org/10.1016/j.tiv.2006.06.012
[12]
Burt, S.A., van der Zee, R., Koets, A.P., de Graaff, A.M., van Knapen, F., Gaastra, W., et al. (2007) Carvacrol Induces Heat Shock Protein 60 and Inhibits Synthesis of Flagellin in Escherichia coli O157:H7. Applied and Environmental Microbiology, 73, 4484-4490. https://doi.org/10.1128/AEM.00340-07
[13]
Blanco, M., Blanco, J.E., Mora, A., Dahbi, G., Alonso, M.P., González, E.A., et al. (2004) Serotypes, Virulence Genes, and Intimin Types of Shiga Toxin (Verotoxin)-Producing Escherichia coli Isolates from Cattle in Spain and Identification of a New Intimin Variant Gene (Eae-ξ). Journal of Clinical Microbiology, 42, 645-651. https://doi.org/10.1128/JCM.42.2.645-651.2004
[14]
Fraser, M.E., Fujinaga, M., Cherney, M.M., Melton-Celsa, A.R., Twiddy, E.M., O’Brien, A.D., et al. (2004) Structure of Shiga Toxin Type 2 (Stx2) from Escherichia coli O157:H7. Journal of Biological Chemistry, 279, 27511-27517. https://doi.org/10.1074/jbc.M401939200
[15]
Friedman, M., Henika, P.R. and Mandrell, R.E. (2002) Bactericidal Activities of Plant Essential Oils and Some of Their Isolated Constituents against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. Journal of Food Protection, 65, 1545-1560. https://doi.org/10.4315/0362-028X-65.10.1545
[16]
Moore-Neibel, K., Gerber, C., Patel, J., Friedman, M. and Ravishankar, S. (2011) Antimicrobial Activity of Lemongrass Oil against Salmonella enterica on Organic Leafy Greens. Journal of Applied Microbiology, 112, 485-492. https://doi.org/10.1111/j.1365-2672.2011.05222.x
[17]
Todd, J., Friedman, M., Patel, J., Jaroni, D. and Ravishankar, S. (2013) The Antimicrobial Effects of Cinnamon Leaf Oil against Multi-Drug Resistant Salmonella Newport on Organic Leafy Greens. International Journal of Food Microbiology, 166, 193-199. https://doi.org/10.1016/j.ijfoodmicro.2013.06.021
[18]
Friedman, M. (2015) Antibiotic-Resistant Bacteria: Prevalence in Food and Inactivation by Food-Compatible Compounds and Plant Extracts. Journal of Agricultural and Food Chemistry, 63, 3805-3822. https://doi.org/10.1021/acs.jafc.5b00778
[19]
Yossa, N., Patel, J., Millner, P., Ravishankar, S. and Lo, Y.M. (2013) Antimicrobial Activity of Plant Essential Oils against Escherichia coli O157:H7 and Salmonella on Lettuce. Foodborne Pathogens and Disease, 10, 87-96. https://doi.org/10.1089/fpd.2012.1301
[20]
Poimenidou, S.V., Bikouli, V.C., Gardeli, C., Mitsi, C., Tarantilis, P.A., Nychas, G.-J., et al. (2016) Effect of Single or Combined Chemical and Natural Antimicrobial Interventions on Escherichia coli O157:H7, Total Microbiota and Color of Packaged Spinach and Lettuce. International Journal of Food Microbiology, 220, 6-18. https://doi.org/10.1016/j.ijfoodmicro.2015.12.013
[21]
Zhu, L., Olsen, C., McHugh, T., Friedman, M., Jaroni, D. and Ravishankar, S. (2014) Apple, Carrot, and Hibiscus Edible Films Containing the Plant Antimicrobials Carvacrol and Cinnamaldehyde Inactivate Salmonella Newport on Organic Leafy Greens in Sealed Plastic Bags. Journal of Food Science, 79, M61-M66. https://doi.org/10.1111/1750-3841.12318
[22]
Zhu, L., Olsen, C., McHugh, T., Friedman, M., Levin, C.E., Jaroni, D., et al. (2020) Edible Films Containing Carvacrol and Cinnamaldehyde Inactivate Escherichia coli O157:H7 on Organic Leafy Greens in Sealed Plastic Bags. Journal of Food Safety, 40, e12758. https://doi.org/10.1111/jfs.12758
[23]
Du, W.-X., Olsen, C.W., Avena-Bustillos, R.J., Friedman, M. and McHugh, T.H. (2011) Physical and Antibacterial Properties of Edible Films Formulated with Apple Skin Polyphenols. Journal of Food Science, 76, M149-M155. https://doi.org/10.1111/j.1750-3841.2010.02012.x
[24]
Espitia, P.J.P., Avena-Bustillos, R.J., Du, W.X., Chiou, B.S., Williams, T.G., Wood, D., et al. (2014) Physical and Antibacterial Properties of Acaí Edible Films Formulated with Thyme Essential Oil and Apple Skin Polyphenols. Journal of Food Science, 79, M903-M910. https://doi.org/10.1111/1750-3841.12432
[25]
Shoji, T., Yamada, M., Miura, T., Nagashima, K., Ogura, K., Inagaki, N., et al. (2017) Chronic Administration of Apple Polyphenols Ameliorates Hyperglycaemia in High-Normal and Borderline Subjects: A Randomised, Placebo-Controlled Trial. Diabetes Research and Clinical Practice, 129, 43-51. https://doi.org/10.1016/j.diabres.2017.03.028
[26]
Shoji, T., Masumoto, S., Moriichi, N., Ohtake, Y. and Kanda, T. (2020) Administration of Apple Polyphenol Supplements for Skin Conditions in Healthy Women: A Randomized, Double-Blind, Placebo-Controlled Clinical Trial. Nutrients, 12, Article No. 1071. https://doi.org/10.3390/nu12041071
[27]
Wang, J., Sun, Y., Tao, D., Wang, S., Li, C., Zheng, F., et al. (2019) Reduction of Escherichia coli O157:H7, Listeria monocytogenes, and Naturally Present Microbe Counts on Lettuce Using an Acid Mixture of Acetic and Lactic Acid. Microorganisms, 7, Article No. 373. https://doi.org/10.3390/microorganisms7100373
[28]
Peixoto, C.M., Dias, M.I., Alves, M.J., Calhelha, R.C., Barros, L., Pinho, S.P., et al. (2018) Grape Pomace as a Source of Phenolic Compounds and Diverse Bioactive Properties. Food Chemistry, 253, 132-138. https://doi.org/10.1016/j.foodchem.2018.01.163
[29]
Friedman, M. (2014) Antibacterial, Antiviral, and Antifungal Properties of Wines and Winery Byproducts in Relation to Their Flavonoid Content. Journal of Agricultural and Food Chemistry, 62, 6025-6042. https://doi.org/10.1021/jf501266s
[30]
Friedman, M., Henika, P.R., Levin, C.E., Mandrell, R.E. and Kozukue, N. (2006) Antimicrobial Activities of Tea Catechins and Theaflavins and Tea Extracts against Bacillus cereus. Journal of Food Protection, 69, 354-361. https://doi.org/10.4315/0362-028X-69.2.354
[31]
Friedman, M. (2007) Overview of Antibacterial, Antitoxin, Antiviral, and Antifungal Activities of Tea Flavonoids and Teas. Molecular Nutrition & Food Research, 51, 116-134. https://doi.org/10.1002/mnfr.200600173
[32]
Friedman, M., Tam, C.C., Cheng, L.W. and Land, K.M. (2020) Anti-Trichomonad Activities of Different Compounds from Foods, Marine Products, and Medicinal Plants: A Review. BMC Complementary Medicine and Therapies, 20, Article No. 271. https://doi.org/10.1186/s12906-020-03061-9
[33]
Friedman, M. (2017) Antimicrobial Activities of Plant Essential Oils and Their Components against Antibiotic-Susceptible and Antibiotic-Resistant Foodborne Pathogens. In: Rai, M., Zachino, S. and Derita, M.D., Eds., Essential Oils and Nanotechnology for Treatment of Microbial Diseases, CRC Press, Boca Raton, 14-38. https://doi.org/10.1201/9781315209241-2
