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Plant Phenolics and Phenolic-Enriched Extracts as Antimicrobial Agents against Food-Contaminating Microorganisms

Miklós Takó, Erika Beáta Kerekes, Carolina Zambrano and 4 more

Antioxidants · 2020 · Review · CC BY

doi:10.3390/antiox9020165

Abstract

Phenolic compounds and extracts with bioactive properties can be obtained from many kinds of plant materials. These natural substances have gained attention in the food research as possible growth inhibitors of foodborne pathogenic and spoilage bacteria. Many phenolic-enriched plant extracts and individual phenolics have promising anti-quorum sensing potential as well and can suppress the biofilm formation and toxin production of food-related pathogens. Various studies have shown that plant phenolics can substitute or support the activity of synthetic food preservatives and disinfectants, which, by the way, can provoke serious concerns in consumers. In this review, we will provide a brief insight into the bioactive properties, i.e., the antimicrobial, anti-quorum sensing, anti-biofilm and anti-enterotoxin activities, of plant phenolic extracts and compounds, with special attention to pathogen microorganisms that have food relation. Carbohydrase aided applications to improve the antimicrobial properties of phenolic extracts are also discussed.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 21, 2026. Paragraph numbers are ours, so an answer can point at one.

1. Introduction

Phenolic compounds are secondary metabolites in plants and are considered as important natural molecules due to their bioactive properties. Phenolics are eliminators of free radicals and metal chelators. They can inhibit the lipid peroxidation and exhibit various physiological activities as antioxidants. In plants, these substances contribute to the defense mechanisms, and adaptation and pigmentation processes. Concerning human health, they have potential in the prevention and treatment of certain chronic diseases such as cardiovascular disease, diabetes and cancer. In addition, plant phenolics and extracts rich in such substances can be excellent inhibitors of many foodborne pathogenic and spoilage bacteria. Various food-related bacteria have biofilm-forming ability and can cause serious contaminations in the food industry. Quorum sensing, as a mechanism of bacterial cell-to-cell chemical communication, plays an important role in biofilm formation, antibiotic resistance, survival, proliferation and toxin production of the pathogens. Inhibition of this signaling process can contribute to the biological control of pathogenic organisms and bacterial toxins causing food deterioration and/or poisoning.

Byproducts of antioxidative plants generated through agro- and food industrial processes are excellent sources of bioactive phenolic materials with antimicrobial effects. Physical and chemical extractions are common methods to obtain these active compounds from plants, but solid-state fermentation and enzyme assisted extraction procedures using carbohydrase active microorganisms or enzymes, can also be useful approaches.

Due to the growing knowledge on their bioactive values, use of plant phenolics as natural additives has recently gained interest in the food industry. Several studies demonstrated the potential of these antioxidant and antimicrobial compounds as food preservatives as well as functional food ingredients. In this respect, phenolic acids, flavonoids and tannins have gained special attention over the last decades.

This review emphasizes the importance of using plant phenolics as natural alternatives of synthetic compounds to eliminate pathogens and spoilage bacteria from food environments. Also, this review deals on the inhibitory potential of phenolic antioxidants against the quorum sensing system, biofilm formation and enterotoxin production of food-related microorganisms. Some studies to improve the phenolic-related antimicrobial activity of plant extracts by using carbohydrases are also highlighted.

2. Foodborne Pathogens and Food Spoilage Organisms

Foodborne diseases constitute a global health problem. During the infection, pathogenic bacteria and/or microbial toxins produced enter to the human body through the contaminated food or water. Pathogenesis varies according to the host’s health conditions, the type of microorganisms and the amount of the agent to which the host is initially exposed. Common examples of food and waterborne outbreaks are the Staphylococcus aureus food poisoning and the Salmonella Typhimurium infection, which cause toxic symptoms and gastrointestinal infection. Table 1 presents some common foodborne pathogenic bacteria, their sources and produced toxins as well as the diseases caused.

Certain food pathogens can survive under adverse environmental factors such as cold, heat, acidic and high salt conditions and have the capacity to form biofilms on biotic or abiotic surfaces. These properties can facilitate their growth and spread on food contact surfaces as well.

On the other hand, the consumption of raw products, such as fruits and vegetables, packaged salads and ready-to-eat products has increased. This can cause diseases by exposing consumers to a greater variety of products potentially contaminated with food pathogens. Moreover, the misuse and overuse of anti-infective drugs against pathogenic microorganisms has generated greater resistance to clinical antibiotic therapy, acquiring the ability to survive at high drug concentration that cause serious diseases and/or chronic infections.

Microbiological deterioration of foods adversely affects their physico-chemical properties and thereby the sensory characteristics. Texture softening, slime production, off-odors, off-flavors and colorization are the main signs of food spoilage. The main spoiling microbes in animal-derived products (e.g., milk, dairy, meat and poultry) are Enterobacteriaceae, lactobacilli, Pseudomonas, Proteus and Brochotrix species. Yeasts and molds, i.e., Saccharomyces, Candida, Pichia, Aspergillus, Penicillium, Botrytis and Fusarium species, and bacteria such as pseudomonads, clostridia, bacilli and Erwinia are common spoilers in plant-derived products.

Prevention and control of foodborne pathogens and spoilers require their detection in the food. Conventional methods rely on culturing of microorganisms on special media allowing their identification and enumeration. These methods are precise but time- and labor-consuming. Some rapid detection method based on nucleic acids sequencing, metabolomics and proteomics have been developed in the recent decades. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) can be used for the identification of pathogens through analysis of the whole cell proteome. Metabolites produced by pathogens or spoilers are detected by means of gas chromatography-mass spectrometry (GC-MS) or electronic nose. Immunological methods, such as the enzyme-linked immunosorbent assay (ELISA), are also used for rapid detection of certain pathogens (e.g., Salmonella). For prevention and control of foodborne microorganisms, physical and chemical methods, like sterilization, pasteurization, irradiation, high hydrostatic pressure or preservatives can be used.

Some of these foodborne pathogenic and spoilage microorganisms became tolerant against the conventional food preservation and conservation methods. There is a significant industrial demand for novel preservation techniques because of the common food losses due to microbial deterioration. Moreover, the consumers’ concern against the chemical preservatives in foods is growing, which also encourages the researchers to find natural alternatives with high antimicrobial potential. These substances then can be used as preservative agents to improve the shelf life of food products. Plant phenolic substances can be promising candidates for these studies.

3. Antimicrobial Activity of Plant Phenolics

Plant-derived phenolics, such as phenolic acids, flavonoids, stilbenes and tannins, can inhibit the growth and activity of many microorganisms, including food-related pathogens as well as clinically important bacteria, fungi and protozoa. Since the different molecules vary in their structure and chemical composition (Figure 1), they can display various antimicrobial effects, such as permeabilization and destabilization of the plasma membrane or inhibition of extracellular enzymes. Moreover, these mechanisms of action differ from those of the traditional antibiotics, which could make plant phenolics effective against drug-resistant pathogens.

Extracts of grape pomace, grape seed, apple, and various exotic fruit and medicinal plant samples are frequently examined for their potential antimicrobial activity. In a pilot research, for instance, the influence of grape pomace extract on the growth of 14 pathogenic and spoilage bacteria was investigated. In agar well diffusion tests, the order of the effective extract concentrations were found to be 20 > 10 > 5 > 2.5 > 1% (w/v), while in serial dilution assays, the sample at 0.5% (w/v) concentration had a bacteriostatic activity against Escherichia coli O157:H7 and S. aureus. In another study, red grape pomace possessed a strong bactericidal effect against E. coli and S. aureus at 12 mg/mL concentration. The growth inhibitory effect, tested at concentrations from 0.5 to 2 mg/mL, varied in a dose dependent manner, and the S. aureus was more susceptible to the grape pomace extract than the E. coli strain tested. Grape seed extracts were also proved to be effective growth suppressors of other food-related bacteria such as S. Typhimurium, Listeria monocytogenes, Bacillus spp., Pseudomonas aeruginosa and Campylobacter spp.. Among exotic fruits, extracts and betacyanin fractions of red pitahaya exhibited a good antimicrobial spectrum against Gram-positive and Gram-negative bacteria, yeasts and molds at concentrations from 7.8 µg/mL to 50 mg/mL. Table 2 summarizes some additional examples about the antimicrobial activity of plant phenolic extracts, indicating the type of extraction and major antimicrobial activity indices.

Studies were also done using plant phenolic extracts as natural preservatives in food systems. The work of Sagdic et al., for instance, was oriented towards in situ studies where they tested the antimicrobial activity of grape pomace extracts in beef patties. Samples from five grape varieties were incorporated to beef patties and the growth of Enterobacteriaceae, coliforms, Salmonella, S. aureus, total aerobic mesophilic count, yeast and molds, lactobacilli and micrococci pathogens was studied in different storage periods. Each pomace extract inhibited the microorganisms in a concertation dependent manner. Pathogenic bacteria, yeasts and molds were completely inhibited by 5 and 10% of the extracts. In another experiment performed in vegetable soup environment, the grape pomace extract showed antibacterial activity in a dose dependent manner against S. aureus and E. coli, due to its high proanthocyanidin content. In meat paté, experiments of Hayrapetyan et al. showed that a flavonoid-rich pomegranate (Punica granatum) peel extract could inhibit the growth of L. monocytogenes by 4.1 log at 4 °C during 46 days, but the inhibitory effect was less effective at higher temperatures (i.e., at 7 and 12 °C), demonstrating the influence of temperature on the inhibitory effect. Ahn et al. added grape seed and pine bark extracts and oleoresin rosemary to ground beef and, after cooking, samples were inoculated with strains of foodborne pathogens (E. coli O157:H7, L. monocytogenes, S. Typhimurium and Aeromonas hydrophila). Pine bark extract at 1% concentration was the most effective against the growth of pathogens after 9 days of storage. Apart from the above studies, there were several experiments on the application of plant phenolic extracts as antimicrobials in various foods (these studies have recently been summarized by Bouarab Chibane et al.).

Individual phenolic compounds of plant extracts have been shown to affect the growth of food-related microorganisms. In the study of García-Ruiz et al., the antimicrobial activity of 18 phenolic compounds, i.e., hydroxycinnamic and hydroxybenzoic acids, stilbenes, flavan-3-ols, flavonols and phenolic alcohols, was evaluated against lactic acid bacteria wine isolates of Oenococcus oeni, Lactobacillus hilgardii and Pediococcus pentosaceus. Among the tested phenolics, the flavonols and stilbenes exhibited the strongest inhibitory effect on bacterial growth. In another experiment, Pastorkova et al. investigated the antimicrobial potential of 15 phenolic compounds (i.e., phenolic acids, stilbenes and flavonoids) naturally occurring in grapes against wine spoilage yeasts and acetic acid bacteria. Pterostilbene, resveratrol and luteolin presented the major inhibitory effects on all tested microorganisms. Phenolic acids, i.e., myricetin, p-coumaric and ferulic acids, showed selective antimicrobial activity depending on the yeast and bacteria species tested. Activity of lignans and flavonoids were tested against E. coli, L. monocytogenes, P. aeruginosa, Klebsiella pneumoniae, Enterobacter cloacae, S. aureus and Enterococcus faecalis in the study of Favela-Hernández et al.. Dihydroguaiaretic acid, 4-epi-larreatricin, 3′-Demethoxy-6-O-demethylisoguaiacin and 5,4′-dihydroxy-7-methoxyflavone compounds showed high growth inhibitory potential towards some of the tested strains, with a MIC range from 12.5 to 50 µg/mL. MIC values of 500–1000 μg/mL were reported for the 7-hydroxycoumarin (umbelliferone) against S. aureus, methicillin-resistant S. aureus (MRSA), E. coli and P. aeruginosa. Table 3 shows other experiments from the last decade testing antimicrobial activity of individual phenolic compounds.

The phenolic compounds can express their microbicide effect through different mode of action. These molecules can suppress several microbial virulence factors (e.g., by inhibition of biofilm formation, reduction of host ligand adhesion and neutralization of bacterial toxins), reduce the fluidity of membrane, inhibit the synthesis of nucleic acids and the cell wall or energy metabolism. In addition, many phenolics could show synergy with antibiotics enhancing their effectiveness and reducing the dose of use. The presence and number of hydroxyl groups in phenolic compounds is responsible for their antioxidant properties. In addition, changes in the position of the hydroxyl group could play an important role in the antimicrobial activity and the interactions with cell membrane structures. In case of carvacrol, for instance, presence of the hydroxyl group and the delocalized electron system are thought to be responsible for the cytoplasmic membrane destabilization and the collapse of the proton motive force that finally led to death of Bacillus cereus cells. Phenolic hydroxyl groups can form hydrogen bonds with active site of enzymes inhibiting their catalytic activity.

Antimicrobial action of phenolics may vary from molecule to molecule. In the study of Engels et al., gallotannins isolated from mango kernel inhibited the growth of Bacillus subtilis and other foodborne pathogens such as S. aureus and E. coli. The inhibitory effects of gallotannins may be attributed to their iron-complexing properties and ability to interact with proteins and inhibit enzyme activities. At the same time, flavonoids have a series of antibacterial actions with different mechanisms of action, such as inhibition of nucleic acid synthesis, induction of cytoplasmic membrane damage and inhibition of energy metabolism, biofilm formation and bacterial toxin production. The flavonoid catechin can penetrate the lipid bilayers of the membrane resulting in leakage of intramembranous materials and liposome aggregation. Moreover, in synergy tests, the catechin-rich fraction of green tea (Camellia sinensis) extracts could reverse the resistance to methicillin in MRSA.

On the other hand, it is possible to increase the antimicrobial activity of plant extracts by certain processes. An ecofriendly way is the treatment with carbohydrase enzymes that can hydrolyze the phenolic glycosides improving the antimicrobial potential of the samples. For instance, Pectinase 62L (10 U polygalacturonase equivalent activity) treatment for two hours at pH 5.0 and 37 °C caused a decrease in the minimum inhibitory concentration (MIC) values of bergamot peel extracts against Salmonella enterica, Pseudomonas putida, E. coli and B. subtilis, compared to the enzyme-free control. The antimicrobial effect against different types of bacteria may depend on the enzyme cocktail(s) used for the treatment as well. In the study of Puupponen-Pimiä et al., different pectinase treatments affected differently the inhibition potential of bilberry extracts against Salmonella and Staphylococcus bacteria. Pectinex Smash, Pectinex BE 3-L and Biopectinase CCM treated samples exhibited the highest antimicrobial activity against the Staphylococcus strains, while Pectinex Ultra SP-L, Pectinex 3 XL and Pectinex BE XXL treatments were superior in case of the Salmonella isolates. For pumpkin and flaxseed extracts, treatment using a mixed cocktail of immobilized Aspergillus oryzae α-amylase, and Aspergillus niger β-glucosidase and β-glucanase enzymes (in a ratio of 1:1:1) resulted in elevated antimicrobial activity against pathogenic bacteria compared to the enzyme-free sample. Red grape pomace subjected to cellulase-assisted extraction efficiently inhibited the growth of E. coli and S. aureus pathogens in the study of Kabir et al..

4. Quorum Sensing Systems and Biofilm Formation in Food Related Bacteria

The quorum sensing system is responsible for the formation of many food deterioration phenotypes. The mechanism regulates important cellular functions such as biofilm formation, sporulation, expression of virulence genes, conjugation, competition, bioluminescence and the production of toxins and pigments. Since the quorum sensing is a density dependent communication mechanism, appearance of the controlled pathological events is related to the density of bacterial cells. The bacterial cells produce and secrete signal molecules, known as autoinducers that accumulate until reaching a sufficient local concentration of bacteria (a quorum) and start a series of population responses, including biofilm formation. The autoinducers secreted by the Gram-negative bacteria are mainly N-acylhomoserine lactone (AHL) molecules (autoinducer-1). The autoinducers in Gram-positive bacteria are peptide compounds (i.e., autoinducer peptides, AIP). Furthermore, both Gram-negative and Gram-positive bacteria could secrete autoinducer 2 (AI-2), which are furanosyl borate diester and similar molecules. Other signaling factors, such as p-coumaroyl-homoserine lactone, unsaturated fatty acids and alkylquinolones are also known. Effective quorum sensing inhibition approaches could be the blocking of the synthesis and the secretion of the autoinducers, the enzymatic degradation of the signal molecules, and the receptor antagonism, in which the antagonist prevents the binding of the signal molecules to response regulator proteins (e.g., to LuxR). However, according to recent investigations, resistance could be developed against certain anti-quorum sensing treatments. Furanones are well-known natural antimicrobials that show destructive activity against the quorum sensing system of both Gram-negative and Gram-positive bacteria.

Biofilms are microbial communities attached to biotic and abiotic surfaces and embedded in a matrix of extracellular polysaccharides, lipids, proteins and nucleic acids, the so called extracellular polymeric substances (EPS) that are produced by the microbial community itself. Inside the biofilm, the cells display different metabolic activity and physiological, gene expression and morphological patterns compared to the planktonic cells. They become more resistant to environmental adverse factors, such as the lack of nutrients and oxygen and changes in the pH condition. Biofilm bacteria are less sensitive to the action of antimicrobial agents causing a potential risk in food industry environments. In addition, the antimicrobial substances at subinhibitory concentration can act as environmental signals activating the formation of biofilms, thereby, leading to the failure of the drug treatment. However, an effective quorum sensing inhibitor could inhibit the biofilm formation of foodborne pathogenic and spoilage bacteria as well. Therefore, in agreement with today’s consumer demands, there are food preservative developments focusing on the screen and extensive analysis of natural inhibitory systems.

5. Anti-Quorum Sensing and Antibiofilm Effects of Plant Phenolics

Certain plant phenolic substances, including phenol-rich crude extracts, could exhibit anti-biofilm and/or anti-quorum sensing activities. The phenolic compounds suppress the bacterial biofilm formation by the inhibition of different regulatory mechanisms without affecting growth: they can block the quorum sensing as mentioned above, reduce the bacterial motility altering their performance, decrease the superficial adhesion and inhibit the expression of virulence factors associated with pathogenic behaviors.

In the study of Vattem et al., the anti-quorum sensing effect of aqueous phenolic extracts from common dietary fruits, herbs and spices was investigated, using the purple pigment violacein producer Chromobacterium violaceum CVO26/CV 31532 bioassay system. The violacein synthesis is under quorum sensing regulation, mediated by AHL autoinducers. Among the fruit extracts tested, raspberry, blueberry and grape samples inhibited the AHL activity, and blueberry had the highest effect on the AHL synthesis. Moreover, blueberry extract was outstanding in the inhibition of quorum sensing related swarming motility in P. aeruginosa and E. coli O157:H7 pathogens. Berry phenolic extracts, namely those from raspberry and cloudberry, were the most effective C. violaceum AHL signaling inhibitors in the study of Priha et al.. In addition, the cloudberry extract reduced the biofilm formation of the common brewery contaminant bacterium, Obesumbacterium proteus at the concentrations of 25 and 50 mg/L. A bioactive phenol-rich extract from apple peel was also tested for its anti-quorum sensing effect in the C. violaceum agar-diffusion test system by Fratianni et al.. The whole extract exhibited quorum sensing inhibiting activity, which, however, was not detected for the single phenolic compounds of the apple peel. Here, the authors pointed out on possible synergistic or combinatory effects between the molecules in the extract, resulting in anti-quorum sensing activity for the crude sample. In a C. violaceum based liquid test, significant inhibition of violacein production was recorded for syringic acid, vanillic acid, (+)-catechin and resveratrol compounds (10 µg/mL), that can be found at different concentrations in black grape, apple and pitahaya extracts. The yield of some of these phenolics, obtained via carbohydrase-assisted extraction, showed positive association with the anti-quorum sensing activity of the crude extracts tested. In the same research, all single phenolic compounds tested, i.e., 4-hydroxybenzoic, syringic, gallic, vanillic, cinnamic and p-coumaric acids, (+)-catechin, (−)-epicatechin, quercetin, polydatin and resveratrol, inhibited the biofilm formation of L. monocytogenes, S. aureus, MRSA, E. coli, S. enterica, P. putida and P. aeruginosa pathogens in vitro, at 100 µg/mL concentration.

In addition, many other studies have addressed the ability of phenolic compounds and different plant extracts to modulate the quorum sensing system and the biofilm formation in foodborne pathogenic and spoilage bacteria. For instance, catechin, naringenin and quercetin depicted strong anti-quorum sensing property against P. aeruginosa. Additionally, flavonoid fraction of guava (Psidium guajava L.) leaves extract inhibited the quorum sensing system of C. violaceum, and the biofilm formation, pyocyanin production, proteolytic and elastolytic activities and swarming motility in P. aeruginosa PAO1. It was shown that the quercetin and quercetin-3-O-arabinoside components of the flavonoid extract were responsible for the anti-quorum sensing activity.

There were several investigations concerning the inhibition of pathogenic E. coli biofilms by phenolics. In the study of Lee et al., the flavonoid phloretin, a major compound in apple and strawberry extracts, has inhibited the formation of E. coli O157:H7 biofilms without affecting the growth of planktonic cells. Two furocoumarins isolated from grapefruit juice, bergamottin and dihydroxybergamottin, suppressed the biofilm formation of E. coli O157:H7 in a range of 71.9 and 58.3%, respectively. Furthermore, naringenin, quercetin, sinensetin and apigenin were effective quorum sensing antagonists and biofilm suppressors in E. coli O157:H7 strain. For non-O157 Shiga toxin producing E. coli strains, Sheng et al. found that the grape seed extract inhibited well the quorum sensing system.

Many phenolic acids proved to be effective against S. aureus biofilms as well. With this context, the gallic, ginkgolic, ellagic and rosmarinic acids have been found to be promising inhibitors in the research of the past decade. The phenolic glycoside compound, 1,2,3,4,6-penta-O-galloyl-β-D-glucopyranose, purified from Eustigma oblongifolium extract, inhibited the formation of S. aureus biofilms by blocking the synthesis of cell-to-cell adhesion compounds, thereby, preventing the primary attachment to solid surfaces. It was also shown that methanol extract from pomegranate, rich in ellagic acid, inhibited the biofilm formation of S. aureus, MRSA, E. coli and C. albicans. Red wines, extensively recognized for their high flavonoid (e.g., quercetin, kaempferol, apigenin, chrysin, fisetin and luteolin) and stilbenoid (e.g., trans-resveratrol) content have proven to be potent inhibitor of S. aureus biofilms. Among the compounds tested, the quercetin exhibited the highest biofilm inhibitory potential. In addition, phenolic extracts from muscadine grape were also able to inhibit and eradicate the S. aureus biofilm in the study of Xu et al.. A summary of some recently published researches about antibiofilm activity of plant extracts against food-related microorganisms is presented in Table 4.

6. Anti-Enterotoxin Effect of Plant Phenolics

Many phenolic compounds and extracts even at concentrations below the MIC can inhibit the production and/or the activity of bacterial enterotoxins. These anti-enterotoxin properties are being intensively tested for foodborne pathogens, especially in case of S. aureus. The staphylococcal enterotoxins and enterotoxin-like molecules are low-molecular weight proteins with a globular structure. They have superantigenic activity and are varied in their emetic potential. Among them, the enterotoxin A is responsible for most staphylococcal food poisoning outbreaks. Phenolic compounds can affect the enterotoxin production through several mode of action, including translation and/or transcription inhibition, disruption of secretory mechanisms, inhibition of quorum sensing regulatory systems, and toxin inactivation. Various plant derived phenolic substances have been described as effective inhibitors of the staphylococcal enterotoxin production and activity (Table 5).

Activity of phenolics on AB-type protein toxins, e.g., cholera toxin, Shiga toxins, E. coli heat-labile toxin, P. aeruginosa exotoxin A, has also been extensively studied. These toxins consist of an A catalytic subunit and a B cell-binding subunit. Grape extracts inhibited the cholera intoxication in cultured cells and intestinal loops through various actions, including the elimination of the pre-bound toxin from the cell surfaces, and disruption of the unfolding, transport and catalytic activities of the dissociated A subunit. In a later study, the function of 20 individual phenolic constituents of grape extracts in cholera toxin inhibition was assessed. Among others, inhibitory functions affecting the toxin binding and the enzyme activity have been associated with the mode of action of individual phenolic compounds. For instance, resveratrol disrupted the toxin internalization and activity, epigallocatechin gallate and procyanidin blocked the toxin binding and occupied the binding sites, and kaempferol and quercitrin could directly inhibit the activity of the catalytic subunit. Grape seed and grape pomace extracts effectively disrupted the action of the Shiga toxin 1 and 2, and the heat-labile toxin as well.

7. Conclusions

Many phenolic compounds and phenol-rich plant extracts have promising activity to inhibit the growth of both the planktonic form and the biofilms of food related pathogens. Investigation of this property is particularly important as bacterial biofilm layers are commonly formed on foods and/or food contact surfaces, resulting in a microbial community more resistant to the traditional disinfectant agents. Moreover, their inhibitory properties against the production and activity of bacterial enterotoxins can make many plant phenolics effective in preventing food poisoning symptoms. Plant phenolics could have anti-quorum sensing activity as well. The quorum sensing mechanism regulates the biofilm formation and toxin production of pathogenic bacteria; therefore, discovery and analysis of substances suppressing this system has also occupied a prominent field in the current researches. In conclusion, the summarized studies emphasize not only the importance of plant phenolic extracts as sources of natural preservatives but provide alternatives for ecofriendly utilization of some agro- and food industrial byproducts and enzyme aided extraction processes as well.

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    Kabir F., Sultana M.S., Kurnianta H. Antimicrobial activities of grape (Vitis vinifera L.) pomace polyphenols as a source of naturally occurring bioactive components. Afr. J. Biotechnol. 2015;14:2157-2161.

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  32. 32.

    Jayaprakasha G.K., Selvi T., Sakariah K.K. Antibacterial and antioxidant activities of grape (Vitis vinifera) seed extracts. Food Res. Int. 2003;36:117-122.

    Not in our library10.1016/s0963-9969(02)00116-3

  33. 33.

    Silván J.M., Mingo E., Hidalgo M., De Pascual-Teresa S., Carrascosa A.V., Martinez-Rodriguez A.J. Antibacterial activity of a grape seed extract and its fractions against Campylobacter spp. Food Control. 2013;29:25-31.

    Not in our library10.1016/j.foodcont.2012.05.063

  34. 34.

    Levy J., Boyer R.R., Neilson A.P., O’Keefe S.F., Chu H.S.S., Williams R.C., Dorenkott M.R., Goodrich K.M. Evaluation of peanut skin and grape seed extracts to inhibit growth of foodborne pathogens. Food Sci. Nutr. 2017;5:1130-1138.

    Not in our library10.1002/fsn3.503

  35. 35.

    Tenore G.C., Novellino E., Basile A. Nutraceutical potential and antioxidant benefits of red pitaya (Hylocereus polyrhizus) extracts. J. Funct. Foods. 2012;4:129-136.

    Not in our library10.1016/j.jff.2011.09.003

  36. 36.

    Yong Y.Y., Dykes G., Lee S.M., Choo W.S. Comparative study of betacyanin profile and antimicrobial activity of red pitahaya (Hylocereus polyrhizus) and red spinach (Amaranthus dubius). Plant Food. Hum. Nutr. 2017;72:41-47.

    Not in our library10.1007/s11130-016-0586-x

  37. 37.

    Tseng A., Zhao Y. Effect of different drying methods and storage time on the retention of bioactive compounds and antibacterial activity of wine grape pomace (Pinot Noir and Merlot). J. Food Sci. 2012;77:H192-H201.

    Not in our library10.1111/j.1750-3841.2012.02840.x

  38. 38.

    Fratianni F., Coppola R., Nazzaro F. Phenolic composition and antimicrobial and antiquorum sensing activity of an ethanolic extract of peels from the apple cultivar annurca. J. Med. Food. 2011;14:957-963.

    Not in our library10.1089/jmf.2010.0170

  39. 39.

    Xu Y., Burton S., Kim C., Sismour E. Phenolic compounds, antioxidant, and antibacterial properties of pomace extracts from four Virginia-grown grape varieties. Food Sci. Nutr. 2016;4:125-133.

    Not in our library10.1002/fsn3.264

  40. 40.

    Usha M., Ragini S., Naqvi S.M.A. Antibacterial activity of acetone and ethanol extracts of cinnamon (Cinnamomum zeylanicum) and Ajowan (Trachyspermum ammi) on four food spoilage bacteria. Int. Res. J. Biol. Sci. 2012;1:7-11.

    Not in our library

  41. 41.

    Salaheen S., Nguyen C., Hewes D., Biswas D. Cheap extraction of antibacterial compounds of berry pomace and their mode of action against the pathogen Campylobacter jejuni. Food Control. 2014;46:174-181.

    Not in our library10.1016/j.foodcont.2014.05.026

  42. 42.

    Shen X., Sun X., Xie Q., Liu H., Zhao Y., Pan Y., Hwang C.-A., Wu V.C.H. Antimicrobial effect of blueberry (Vaccinium corymbosum L.) extracts against the growth of Listeria monocytogenes and Salmonella Enteritidis. Food Control. 2014;35:159-165.

    Not in our library10.1016/j.foodcont.2013.06.040

  43. 43.

    Zhang T., Wei X., Miao Z., Hassan H., Song Y., Fan M. Screening for antioxidant and antibacterial activities of phenolics from Golden Delicious apple pomace. Chem. Cent. J. 2016;10:47.

    Not in our library10.1186/s13065-016-0195-7

  44. 44.

    Ju J., Xie Y., Guo Y., Cheng Y., Qian H., Yao W. Antibacterial activities of bayberry extract on foodborne pathogens and identification of its active components. Food Agric. Immunol. 2019;30:385-397.

    Not in our library10.1080/09540105.2019.1589427

  45. 45.

    Luchian C.E., Cotea V.V., Vlase L., Toiu A.M., Colibaba L.C., Răschip I.E., Nadăş G., Gheldiu A.M., Tuchiluş C., Rotaru L. Antioxidant and antimicrobial effects of grape pomace extracts. BIO Web Conf. 2019;15:04006.

    Not in our library10.1051/bioconf/20191504006

  46. 46.

    Radovanović V.N., Andjelković M., Arsić B., Radovanović A., Gojković-Bukarica L. Cost-effective ultrasonic extraction of bioactive polyphenols from vine and wine waste in Serbia. S. Afr. J. Enol. Vitic. 2019;40:172-180.

    Not in our library10.21548/40-2-3215

  47. 47.

    Olejar K.J., Ricci A., Swift S., Zujovic Z., Gordon K.C., Fedrizzi B., Versari A., Kilmartin P.A. Characterization of an antioxidant and antimicrobial extract from cool climate, white grape marc. Antioxidants. 2019;8:232.

    Not in our library10.3390/antiox8070232

  48. 48.

    Raphaelli C.O., Dannenberg G., Dalmazo G.O., Pereira E.S., Radünz M., Vizzotto M., Fiorentini A.M., Gandra E.A., Nora L. Antibacterial and antioxidant properties of phenolic-rich extracts from apple (Malus domestica cv. Gala). Int. Food Res. J. 2019;26:1133-1142.

    Not in our library

  49. 49.

    Mahboubi A., Asgarpanah J., Sadaghiyani P.N., Faizi M. Total phenolic and flavonoid content and antibacterial activity of Punica granatum L. var. pleniflora flowers (Golnar) against bacterial strains causing foodborne diseases. BMC Complement. Altern. Med. 2015;15:366.

    Not in our library10.1186/s12906-015-0887-x

  50. 50.

    Al-Manhel A.J., Niamah A.K. Effect of aqueous and alcoholic plant extracts on inhibition of some types of microbes and causing spoilage of food. J. Nutr. Food. Sci. 2015;S5:104-109.

    Not in our library10.4172/2155-9600.s5-006

  51. 51.

    Arokiyaraj S., Bharanidharan R., Agastian P., Shin H. Chemical composition, antioxidant activity and antibacterial mechanism of action from Marsilea minuta leaf hexane: Methanol extract. Chem. Cent. J. 2018;12:105.

    Not in our library10.1186/s13065-018-0476-4

  52. 52.
  53. 53.

    Ibrahim M.M., El Ghani S.A., El-Moez S.I.A. Phytochemical analysis and antimicrobial activities of different callus extracts of Pelargonium sidoides DC. against food borne pathogenic bacteria. J. Appl. Pharm. Sci. 2018;8:109-118.

    Not in our library

  54. 54.

    Generalić Mekinić I., Skroza D., Ljubenkov I., Katalinić V., Šimat V. Antioxidant and antimicrobial potential of phenolic metabolites from traditionally used Mediterranean herbs and spices. Foods. 2019;8:579.

    Not in our library10.3390/foods8110579

  55. 55.

    Nas F.S., Ali M., Ahmad A.M. In vitro antibacterial activity of different extracts of Zingiber officinale against bacterial isolates responsible for food spoilage. SOA Arch. Pharm. Pharmacol. 2018;1:001.

    Not in our library

  56. 56.

    Ouerghemmi I., Rebey I.B., Rahali F.Z., Bourgou S., Pistelli L., Ksouri R., Marzouk B., Tounsi M.S. Antioxidant and antimicrobial phenolic compounds from extracts of cultivated and wild-grown Tunisian Ruta chalepensis. J. Food Drug Anal. 2017;25:350-359.

    Not in our library10.1016/j.jfda.2016.04.001

  57. 57.

    Ramli S., Radu S., Shaari K., Rukayadi Y. Antibacterial activity of ethanolic extract of Syzygium polyanthum L. (Salam) leaves against foodborne pathogens and application as food sanitizer. BioMed Res. Int. 2017;2017:9024246.

    Not in our library10.1155/2017/9024246

  58. 58.

    Sagdic O., Ozturk I., Yilmaz M.T., Yetim H. Effect of grape pomace extracts obtained from different grape varieties on microbial quality of beef patty. J. Food Sci. 2011;76:M515-M521.

    Not in our library10.1111/j.1750-3841.2011.02323.x

  59. 59.

    Sagdic O., Ozturk I., Kisi O. Modeling antimicrobial effect of different grape pomace and extracts on S. aureus and E. coli in vegetable soup using artificial neural network and fuzzy logic system. Expert Syst. Appl. 2012;39:6792-6798.

    Not in our library10.1016/j.eswa.2011.12.047

  60. 60.

    Hayrapetyan H., Hazeleger W.C., Beumer R.R. Inhibition of Listeria monocytogenes by pomegranate (Punica granatum) peel extract in meat paté at different temperatures. Food Control. 2012;23:66-72.

    Not in our library10.1016/j.foodcont.2011.06.012

  61. 61.

    Ahn J., Grün I.U., Mustapha A. Effects of plant extracts on microbial growth, color change, and lipid oxidation in cooked beef. Food Microbiol. 2007;24:7-14.

    Not in our library10.1016/j.fm.2006.04.006

  62. 62.

    Bouarab Chibane L., Degraeve P., Ferhout H., Bouajila J., Oulahal N. Plant antimicrobial polyphenols as potential natural food preservatives. J. Sci. Food Agric. 2019;99:1457-1474.

    Not in our library10.1002/jsfa.9357

  63. 63.

    García-Ruiz A., Moreno-Arribas M.V., Martín-Álvarez P.J., Bartolomé B. Comparative study of the inhibitory effects of wine polyphenols on the growth of enological lactic acid bacteria. Int. J. Food Microbiol. 2011;145:426-431.

    Not in our library10.1016/j.ijfoodmicro.2011.01.016

  64. 64.

    Pastorkova E., Zakova T., Landa P., Novakova J., Vadlejch J., Kokoska L. Growth inhibitory effect of grape phenolics against wine spoilage yeasts and acetic acid bacteria. Int. J. Food Microbiol. 2013;161:209-213.

    Not in our library10.1016/j.ijfoodmicro.2012.12.018

  65. 65.

    Favela-Hernández J.M.J., García A., Garza-González E., Rivas-Galindo V.M., Camacho-Corona M.R. Antibacterial and antimycobacterial lignans and flavonoids from Larrea tridentata. Phytother. Res. 2012;26:1957-1960.

    Not in our library10.1002/ptr.4660

  66. 66.

    Rehman S.-U., Khan R., Bhat K.A., Raja A.F., Shawl A.S., Alam M.S. Isolation, characterisation and antibacterial activity studies of coumarins from Rhododendron lepidotum Wall. ex G. Don, Ericaceae. Rev. Bras. Farmacogn. 2010;20:886-890.

    Not in our library10.1590/s0102-695x2010005000037

  67. 67.

    Nitiema L.W., Savadogo A., Simpore J., Dianou D., Traore A.S. In vitro antimicrobial activity of some phenolic compounds (coumarin and quercetin) against gastroenteritis bacterial strains. Int. J. Microbiol. Res. 2012;3:183-187.

    Not in our library

  68. 68.

    Díaz-Gómez R., Toledo-Araya H., López-Solís R., Obreque-Slier E. Combined effect of gallic acid and catechin against Escherichia coli. LWT Food Sci. Technol. 2014;59:896-900.

    Not in our library10.1016/j.lwt.2014.06.049

  69. 69.

    Kerekes E.B., Vidács A., Jenei Török 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.

    Not in our library10.1556/018.67.2016.3.10

  70. 70.

    Rúa J., Fernandez-Alvarez L., Gutierrez-Larrainzar M., Del Valle P., De Arriaga D., García-Armesto M.R. Screening of phenolic antioxidants for their inhibitory activity against foodborne Staphylococcus aureus strains. Foodborne Pathog. Dis. 2010;7:695-705.

    Not in our library10.1089/fpd.2009.0440

  71. 71.

    Quideau S., Deffieux D., Douat-Casassus C., Pouységu L. Plant polyphenols: Chemical properties, biological activities, and synthesis. Angew. Chem. Int. Ed. Engl. 2011;50:586-621.

    Not in our library10.1002/anie.201000044

  72. 72.
  73. 73.

    Stefanović O.D., Kırmusaoğlu S. Synergistic activity of antibiotics and bioactive plant extracts: A study against Gram-positive and Gram-negative bacteria. Bacterial Pathogenesis and Antibacterial Control. 2018;23-48.

    Not in our library

  74. 74.
  75. 75.

    Figueiredo A.R., Campos F., De Freitas V., Hogg T., Couto J.A. Effect of phenolic aldehydes and flavonoids on growth and inactivation of Oenococcus oeni and Lactobacillus hilgardii. Food Microbiol. 2008;25:105-112.

    Not in our library10.1016/j.fm.2007.07.004

  76. 76.
  77. 77.

    Ultee A., Bennik M.H.J., Moezelaar R. The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl. Environ. Microbiol. 2002;68:1561-1568.

    Not in our library10.1128/aem.68.4.1561-1568.2002

  78. 78.

    Jeong K.-W., Lee J.-Y., Kang D.-I., Lee J.-U., Shin S.Y., Kim Y. Screening of flavonoids as candidate antibiotics against Enterococcus faecalis. J. Nat. Prod. 2009;72:719-724.

    Not in our library10.1021/np800698d

  79. 79.

    Engels C., Knödler M., Zhao Y.-Y., Carle R., Gänzle M.G., Schieber A. Antimicrobial activity of gallotannins isolated from mango (Mangifera indica L.) kernels. J. Agric. Food Chem. 2009;57:7712-7718.

    Not in our library10.1021/jf901621m

  80. 80.

    Wu T., Zang X., He M., Pan S., Xu X. Structure–activity relationship of flavonoids on their anti-Escherichia coli activity and inhibition of DNA gyrase. J. Agric. Food Chem. 2013;61:8185-8190.

    Not in our library10.1021/jf402222v

  81. 81.
  82. 82.

    Sanver D., Murray B.S., Sadeghpour A., Rappolt M., Nelson A.L. Experimental modeling of flavonoid–biomembrane interactions. Langmuir. 2016;32:13234-13243.

    Not in our library10.1021/acs.langmuir.6b02219

  83. 83.

    Eumkeb G., Chukrathok S. Synergistic activity and mechanism of action of ceftazidime and apigenin combination against ceftazidime-resistant Enterobacter cloacae. Phytomedicine. 2013;20:262-269.

    Not in our library10.1016/j.phymed.2012.10.008

  84. 84.

    Soromou L.W., Zhang Y., Cui Y., Wei M., Chen N., Yang X., Huo M., Baldé A., Guan S., Deng X., et al. Subinhibitory concentrations of pinocembrin exert anti-Staphylococcus aureus activity by reducing α-toxin expression. J. Appl. Microbiol. 2013;115:41-49.

    Not in our library10.1111/jam.12221

  85. 85.

    Ikigai H., Nakae T., Hara Y., Shimamura T. Bactericidal catechins damage the lipid bilayer. BBA Biomembr. 1993;1147:132-136.

    Not in our library10.1016/0005-2736(93)90323-r

  86. 86.

    Taylor P.W., Hamilton-Miller J.M., Stapleton P.D. Antimicrobial properties of green tea catechins. Food Sci. Technol. Bull. 2005;2:71-81.

    Not in our library10.1616/1476-2137.14184

  87. 87.

    Yam T.S., Hamilton-Miller J.M., Shah S. The effect of a component of tea (Camellia sinensis) on methicillin resistance, PBP2′synthesis, and beta-lactamase production in Staphylococcus aureus. J. Antimicrob. Chemother. 1998;42:211-216.

    Not in our library10.1093/jac/42.2.211

  88. 88.

    Mandalari G., Bennett R.N., Bisignano G., Trombetta D., Saija A., Faulds C.B., Gasson M.J., Narbad A. Antimicrobial activity of flavonoids extracted from bergamot (Citrus bergamia Risso) peel, a byproduct of the essential oil industry. J. Appl. Microbiol. 2007;103:2056-2064.

    Not in our library10.1111/j.1365-2672.2007.03456.x

  89. 89.

    Puupponen-Pimiä R., Nohynek L., Ammann S., Oksman-Caldentey K.-M., Buchert J. Enzyme-assisted processing increases antimicrobial and antioxidant activity of bilberry. J. Agric. Food Chem. 2008;56:681-688.

    Not in our library10.1021/jf072001h

  90. 90.

    Ratz-Łyko A., Arct J. Evaluation of antioxidant and antimicrobial properties of enzymatically hydrolysed Cucurbita pepo and Linum usitatissimum seedcakes. Food Sci. Biotechnol. 2015;24:1789-1796.

    Not in our library10.1007/s10068-015-0233-6

  91. 91.

    Skandamis P.N., Nychas G.-J.E. Quorum sensing in the context of food microbiology. Appl. Environ. Microbiol. 2012;78:5473-5482.

    Not in our library10.1128/aem.00468-12

  92. 92.
  93. 93.

    Schaefer A.L., Greenberg E.P., Oliver C.M., Oda Y., Huang J.J., Bittan-Banin G., Peres C.M., Schmidt S., Juhaszova K., Sufrin J.R., et al. A new class of homoserine lactone quorum-sensing signals. Nature. 2008;454:595-599.

    Not in our library10.1038/nature07088

  94. 94.

    Ryan R.P., McCarthy Y., Watt S.A., Niehaus K., Dow J.M. Intraspecies signaling involving the diffusible signal factor BDSF (cis-2-dodecenoic acid) influences virulence in Burkholderia cenocepacia. J. Bacteriol. 2009;191:5013-5019.

    Not in our library10.1128/jb.00473-09

  95. 95.

    Liu Y.-C., Hussain F., Negm O., Paiva A.C., Halliday N., Dubern J.-F., Singh S., Muntaka S., Wheldon L., Luckett J., et al. Contribution of the alkylquinolone quorum-sensing system to the interaction of Pseudomonas aeruginosa with bronchial epithelial cells. Front. Microbiol. 2018;9:3018.

    Not in our library10.3389/fmicb.2018.03018

  96. 96.

    Krzyżek P. Challenges and limitations of anti-quorum sensing therapies. Front. Microbiol. 2019;10:2473.

    Not in our library10.3389/fmicb.2019.02473

  97. 97.

    Lönn-Stensrud J., Landin M.A., Benneche T., Petersen F.C., Scheie A.A. Furanones, potential agents for preventing Staphylococcus epidermidis biofilm infections? J. Antimicrob. Chemother. 2009;63:309-316.

    Not in our library10.1093/jac/dkn501

  98. 98.

    Husain A., Khan S.A., Iram F., Iqbal M.A., Asif M. Insights into the chemistry and therapeutic potential of furanones: A versatile pharmacophore. Eur. J. Med. Chem. 2019;171:66-92.

    Not in our library10.1016/j.ejmech.2019.03.021

  99. 99.
  100. 100.

    Hoffman L.R., D’Argenio D.A., MacCoss M.J., Zhang Z., Jones R.A., Miller S.I. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature. 2005;436:1171-1175.

    Not in our library10.1038/nature03912

  101. 101.
  102. 102.

    Brackman G., Coenye T. Quorum sensing inhibitors as anti-biofilm agents. Curr. Pharm. Des. 2015;21:5-11.

    Not in our library10.2174/1381612820666140905114627

  103. 103.
  104. 104.

    Machado I., Silva L.R., Giaouris E.D., Melo L.F., Simões M. Quorum sensing in food spoilage and natural-based strategies for its inhibition. Food Res. Int. 2020;127:108754.

    Not in our library10.1016/j.foodres.2019.108754

  105. 105.

    Silva L.N., Zimmer K.R., Macedo A.J., Trentin D.S. Plant natural products targeting bacterial virulence factors. Chem. Rev. 2016;116:9162-9236.

    Not in our library10.1021/acs.chemrev.6b00184

  106. 106.
  107. 107.

    Asfour H.Z. Anti-quorum sensing natural compounds. J. Microsc. Ultrastruct. 2018;6:1-10.

    Not in our library10.4103/jmau.jmau_10_18

  108. 108.

    Borges A., Saavedra M.J., Simões M. The activity of ferulic and gallic acids in biofilm prevention and control of pathogenic bacteria. Biofouling. 2012;28:755-767.

    Not in our library10.1080/08927014.2012.706751

  109. 109.

    Eydelnant I.A., Tufenkji N. Cranberry derived proanthocyanidins reduce bacterial adhesion to selected biomaterials. Langmuir. 2008;24:10273-10281.

    Not in our library10.1021/la801525d

  110. 110.

    Xu X., Zhou X.D., Wu C.D. The tea catechin epigallocatechin gallate suppresses cariogenic virulence factors of Streptococcus mutans. Antimicrob. Agents Chemother. 2011;55:1229-1236.

    Not in our library10.1128/aac.01016-10

  111. 111.

    Khokhani D., Zhang C., Li Y., Wang Q., Zeng Q., Yamazaki A., Hutchins W., Zhou S.-S., Chen X., Yang C.-H. Discovery of plant phenolic compounds that act as type III secretion system inhibitors or inducers of the fire blight pathogen, Erwinia amylovora. Appl. Environ. Microbiol. 2013;79:5424-5436.

    Not in our library10.1128/aem.00845-13

  112. 112.

    Vattem D.A., Mihalik K., Crixell S.H., McLean R.J.C. Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia. 2007;78:302-310.

    Not in our library10.1016/j.fitote.2007.03.009

  113. 113.

    Priha O., Virkajärvi V., Juvonen R., Puupponen-Pimiä R., Nohynek L., Alakurtti S., Pirttimaa M., Storgårds E. Quorum sensing signalling and biofilm formation of brewery-derived bacteria, and inhibition of signalling by natural compounds. Curr. Microbiol. 2014;69:617-627.

    Not in our library10.1007/s00284-014-0627-3

  114. 114.

    Vandeputte O.M., Kiendrebeogo M., Rajaonson S., Diallo B., Mol A., El Jaziri M., Baucher M. Identification of catechin as one of the flavonoids from Combretum albiflorum bark extract that reduces the production of quorum-sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 2010;76:243-253.

    Not in our library10.1128/aem.01059-09

  115. 115.

    Vandeputte O.M., Kiendrebeogo M., Rasamiravaka T., Stévigny C., Duez P., Rajaonson S., Diallo B., Mol A., Baucher M., El Jaziri M. The flavanone naringenin reduces the production of quorum sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Microbiology. 2011;157:2120-2132.

    Not in our library10.1099/mic.0.049338-0

  116. 116.

    Ouyang J., Sun F., Feng W., Sun Y., Qiu X., Xiong L., Liu Y., Chen Y. Quercetin is an effective inhibitor of quorum sensing, biofilm formation and virulence factors in Pseudomonas aeruginosa. J. Appl. Microbiol. 2016;120:966-974.

    Not in our library10.1111/jam.13073

  117. 117.

    Vasavi H.S., Arun A.B., Rekha P.-D. Anti-quorum sensing activity of Psidium guajava L. flavonoids against Chromobacterium violaceum and Pseudomonas aeruginosa PAO1. Microbiol. Immunol. 2014;58:286-293.

    Not in our library10.1111/1348-0421.12150

  118. 118.

    Lee J.-H., Regmi S.C., Kim J.-A., Cho M.H., Yun H., Lee C.-S., Lee J. Apple flavonoid phloretin inhibits Escherichia coli O157: H7 biofilm formation and ameliorates colon inflammation in rats. Infect. Immun. 2011;79:4819-4827.

    Not in our library10.1128/iai.05580-11

  119. 119.

    Girennavar B., Cepeda M.L., Soni K.A., Vikram A., Jesudhasan P., Jayaprakasha G.K., Pillai S.D., Patil B.S. Grapefruit juice and its furocoumarins inhibits autoinducer signaling and biofilm formation in bacteria. Int. J. Food Microbiol. 2008;125:204-208.

    Not in our library10.1016/j.ijfoodmicro.2008.03.028

  120. 120.

    Vikram A., Jayaprakasha G.K., Jesudhasan P.R., Pillai S.D., Patil B.S. Suppression of bacterial cell-cell signalling, biofilm formation and type III secretion system by citrus flavonoids. J. Appl. Microbiol. 2010;109:515-527.

    Not in our library10.1111/j.1365-2672.2010.04677.x

  121. 121.

    Sheng L., Olsen S.A., Hu J., Yue W., Means W.J., Zhu M.J. Inhibitory effects of grape seed extract on growth, quorum sensing, and virulence factors of CDC “top-six” non-O157 Shiga toxin producing E. coli. Int. J. Food Microbiol. 2016;229:24-32.

    Not in our library10.1016/j.ijfoodmicro.2016.04.001

  122. 122.

    Luís Â., Silva F., Sousa S., Duarte A.P., Domingues F. Antistaphylococcal and biofilm inhibitory activities of gallic, caffeic, and chlorogenic acids. Biofouling. 2014;30:69-79.

    Not in our library10.1080/08927014.2013.845878

  123. 123.

    Lee J.-H., Kim Y.-G., Ryu S.Y., Cho M.H., Lee J. Ginkgolic acids and Ginkgo biloba extract inhibit Escherichia coli O157: H7 and Staphylococcus aureus biofilm formation. Int. J. Food Microbiol. 2014;174:47-55.

    Not in our library10.1016/j.ijfoodmicro.2013.12.030

  124. 124.

    Bakkiyaraj D., Nandhini J.R., Malathy B., Pandian S.K. The anti-biofilm potential of pomegranate (Punica granatum L.) extract against human bacterial and fungal pathogens. Biofouling. 2013;29:929-937.

    Not in our library10.1080/08927014.2013.820825

  125. 125.

    Slobodníková L., Fialová S., Hupková H., Grančai D. Rosmarinic acid interaction with planktonic and biofilm Staphylococcus aureus. Nat. Prod. Commun. 2013;8:1747-1750.

    Not in our library10.1177/1934578x1300801223

  126. 126.

    Lin M.-H., Chang F.-R., Hua M.-Y., Wu Y.-C., Liu S.-T. Inhibitory effects of 1,2,3,4,6-penta-O-galloyl-β-D-glucopyranose on biofilm formation by Staphylococcus aureus. Antimicrob. Agents Chemother. 2011;55:1021-1027.

    Not in our library10.1128/aac.00843-10

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    Cho H.S., Lee J.-H., Cho M.H., Lee J. Red wines and flavonoids diminish Staphylococcus aureus virulence with anti-biofilm and anti-hemolytic activities. Biofouling. 2015;31:1-11.

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    Xu C., Yagiz Y., Hsu W.-Y., Simonne A., Lu J., Marshall M.R. Antioxidant, antibacterial, and antibiofilm properties of polyphenols from muscadine grape (Vitis rotundifolia Michx.) pomace against selected foodborne pathogens. J. Agric. Food Chem. 2014;62:6640-6649.

    Not in our library10.1021/jf501073q

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    Rahman M.R.T., Lou Z., Yu F., Wang P., Wang H. Anti-quorum sensing and anti-biofilm activity of Amomum tsaoko (Amommum tsao-ko Crevost et Lemarie) on foodborne pathogens. Saudi J. Biol. Sci. 2017;24:324-330.

    Not in our library10.1016/j.sjbs.2015.09.034

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    De Marco S., Piccioni M., Pagiotti R., Pietrella D. Antibiofilm and antioxidant activity of propolis and bud poplar resins versus Pseudomonas aeruginosa. Evid. Based Complement. Altern. Med. 2017;2017:5163575.

    Not in our library10.1155/2017/5163575

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    Maia D.S.V., Haubert L., Kroning I.S., Dos Santos Soares K., Oliveira T.L., Da Silva W.P. Biofilm formation by Staphylococcus aureus isolated from food poisoning outbreaks and effect of Butia odorata Barb. Rodr. extract on planktonic and biofilm cells. LWT Food Sci. Technol. 2020;117:108685.

    Not in our library10.1016/j.lwt.2019.108685

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    Sharma K., Mahato N., Lee Y.R. Systematic study on active compounds as antibacterial and antibiofilm agent in aging onions. J. Food Drug Anal. 2018;26:518-528.

    Not in our library10.1016/j.jfda.2017.06.009

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    Edziri H., Jaziri R., Chehab H., Verschaeve L., Flamini G., Boujnah D., Hammami M., Aouni M., Mastouri M. A comparative study on chemical composition, antibiofilm and biological activities of leaves extracts of four Tunisian olive cultivars. Heliyon. 2019;5:e01604.

    Not in our library10.1016/j.heliyon.2019.e01604

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    Nassima B., Nassima B., Riadh K. Antimicrobial and antibiofilm activities of phenolic compounds extracted from Populus nigra and Populus alba buds (Algeria). Braz. J. Pharm. Sci. 2019;55:e18114.

    Not in our library10.1590/s2175-97902019000218114

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    Blando F., Russo R., Negro C., De Bellis L., Frassinetti S. Antimicrobial and antibiofilm activity against Staphylococcus aureus of Opuntia ficus-indica (L.) Mill. cladode polyphenolic extracts. Antioxidants. 2019;8:117.

    Not in our library10.3390/antiox8050117

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    Famuyide I.M., Aro A.O., Fasina F.O., Eloff J.N., McGaw L.J. Antibacterial and antibiofilm activity of acetone leaf extracts of nine under-investigated south African Eugenia and Syzygium (Myrtaceae) species and their selectivity indices. BMC Complement. Altern. Med. 2019;19:141.

    Not in our library10.1186/s12906-019-2547-z

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    Radojević I.D., Branković S.R., Vasić S.M., Ćirić A.R., Topuzović M.D., Čomić L.R. Phytochemical profiles, antioxidant and antimicrobial with antibiofilm activities of wild growing Potentilla visianii extracts. Nat. Prod. Commun. 2018;13:851-854.

    Not in our library10.1177/1934578x1801300716

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    Stefanović O., Ličina B., Vasić S., Radojević I., Čomić L. Bioactive extracts of Gentiana asclepiadea: Antioxidant, antimicrobial, and antibiofilm activity. Bot. Serbica. 2018;42:223-229.

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    Muñoz-Cazares N., García-Contreras R., Pérez-López M., Castillo-Juárez I., Marcos Soto-Hernandez M., Palma-Tenango M., Del Rosario Garcia-Mateos M. Phenolic compounds with anti-virulence properties. Phenolic Compounds-Biological Activity. 2017;139-167.

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    Albano M., Alves F.C.B., Andrade B.F.M.T., Barbosa L.N., Pereira A.F.M., Da Cunha M., Rall V.L.M., Júnior A.F. Antibacterial and anti-staphylococcal enterotoxin activities of phenolic compounds. Innov. Food Sci. Emerg. Technol. 2016;38:83-90.

    Not in our library10.1016/j.ifset.2016.09.003

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    Rasooly R., Molnar A., Choi H.-Y., Do P., Racicot K., Apostolidis E. In-vitro inhibition of staphylococcal pathogenesis by witch-hazel and green tea extracts. Antibiotics. 2019;8:244.

    Not in our library10.3390/antibiotics8040244

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    Qiu J., Feng H., Xiang H., Wang D., Xia L., Jiang Y., Song K., Lu J., Yu L., Deng X. Influence of subinhibitory concentrations of licochalcone A on the secretion of enterotoxins A and B by Staphylococcus aureus. FEMS Microbiol. Lett. 2010;307:135-141.

    Not in our library10.1111/j.1574-6968.2010.01973.x

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    Souza E.L., Oliveira C.E.V., Stamford T.L.M., Conceição M.L., Gomes Neto N.J. Influence of carvacrol and thymol on the physiological attributes, enterotoxin production and surface characteristics of Staphylococcus aureus strains isolated from foods. Braz. J. Microbiol. 2013;44:29-36.

    Not in our library10.1590/s1517-83822013005000001

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    Shimamura Y., Hirai C., Sugiyama Y., Shibata M., Ozaki J., Murata M., Ohashi N., Masuda S. Inhibitory effects of food additives derived from polyphenols on staphylococcal enterotoxin A production and biofilm formation by Staphylococcus aureus. Biosci. Biotechnol. Biochem. 2017;81:2346-2352.

    Not in our library10.1080/09168451.2017.1395681

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    Zhao Y., Zhu A., Tang J., Tang C., Chen J. Comparative effects of food preservatives on the production of staphylococcal enterotoxin I from Staphylococcus aureus isolate. J. Food Qual. 2017;2017:9495314.

    Not in our library10.1155/2017/9495314

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    Rasooly R., Do P.M., Friedman M. Inhibition of biological activity of staphylococcal enterotoxin A (SEA) by apple juice and apple polyphenols. J. Agric. Food Chem. 2010;58:5421-5426.

    Not in our library10.1021/jf904021b

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    Braga L.C., Shupp J.W., Cummings C., Jett M., Takahashi J.A., Carmo L.S., Chartone-Souza E., Nascimento A.M.A. Pomegranate extract inhibits Staphylococcus aureus growth and subsequent enterotoxin production. J. Ethnopharmacol. 2005;96:335-339.

    Not in our library10.1016/j.jep.2004.08.034

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    Tranter H.S., Tassou S.C., Nychas G.J. The effect of the olive phenolic compound, oleuropein, on growth and enterotoxin B production by Staphylococcus aureus. J. Appl. Bacteriol. 1993;74:253-259.

    Not in our library10.1111/j.1365-2672.1993.tb03023.x

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    Reddy S., Taylor M., Zhao M., Cherubin P., Geden S., Ray S., Francis D., Teter K. Grape extracts inhibit multiple events in the cell biology of cholera intoxication. PLoS ONE. 2013;8:e73390.

    Not in our library10.1371/journal.pone.0073390

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    Cherubin P., Garcia M.C., Curtis D., Britt C.B., Craft J.W., Burress H., Berndt C., Reddy S., Guyette J., Zheng T., et al. Inhibition of cholera toxin and other AB toxins by polyphenolic compounds. PLoS ONE. 2016;11:e0166477.

    Not in our library10.1371/journal.pone.0166477

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    Quiñones B., Massey S., Friedman M., Swimley M.S., Teter K. Novel cell-based method to detect Shiga toxin 2 from Escherichia coli O157: H7 and inhibitors of toxin activity. Appl. Environ. Microbiol. 2009;75:1410-1416.

    Not in our library10.1128/aem.02230-08

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