Antibacterial, Antiviral, and Antifungal Properties of ... - ACS Publications

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Antibacterial, Antiviral, and Antifungal Properties of Wines and Winery Byproducts in Relation to Their Flavonoid Content Mendel Friedman* Western Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture, Albany, California 94710, United States ABSTRACT: Grapes produce organic compounds that may be involved in the defense of the plants against invading phytopathogens. These metabolites include numerous phenolic compounds that are also active against human pathogens. Grapes are used to produce a variety of wines, grape juices, and raisins. Grape pomace, seeds, and skins, the remains of the grapes that are a byproduct of winemaking, also contain numerous bioactive compounds that differ from those found in grapes and wines. This overview surveys and interprets our present knowledge of the activities of wines and winery byproducts and some of their bioactive components against foodborne (Bacillus cereus, Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, Salmonella enterica, Staphylococcus aureus, Yersinia enterocolitica, Vibrio cholerae, Vibrio vulnificus), medical (Helicobacter pylori, Klebsiella pneumoniae), and oral pathogenic bacteria, viruses (adeno, cytomegalo, hepatitis, noro, rota), fungi (Candida albicans, Botrytis cinerea), parasites (Eimeria tenella, Trichomonas vaginalis), and microbial toxins (ochratoxin A, Shiga toxin) in culture, in vivo, and in/on food (beef, chicken, frankfurters, hot dogs, lettuce, oysters, peppers, pork, sausages, soup, spinach) in relation to composition and sensory properties. Also covered are antimicrobial wine marinades, antioxidative and immunostimulating aspects, and adverse effects associated with wine consumption. The collated information and suggested research needs might facilitate and guide further studies needed to optimize the use of wines and byproducts to help improve microbial food safety and prevent or treat animal and human infections. KEYWORDS: adverse effects, antibacterial, antibiotic properties, antifungal, antiinflammatory effects, antioxidative effects, antiviral, flavonoids, food, grape pomace, grape seeds, grape skins, grapevine leaves and stems, human infections, immunostimulating effects, microbial food safety, microbial toxins, oral bacteria, parasites, pathogens, research needs, sensory properties, wine, wine byproducts, wine compostion, wine marinades

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INTRODUCTION Grapes are the second largest fruit crop in the world after oranges. According to the Food and Agricultural Organization of the United Nations, >67 million tons of grapes is produced annually worldwide, with the United States contributing about 10% to the total.1 Wines are classified into major groups, table wines with an alcohol content dealcoholized wine > ethanol at low pH > low pH > ethanol, suggesting the antimicrobial efficacy of wine cannot be attributed to a specific component.130 The average TPC of these wines (in mg GAE/L) was 3204; flavonoids, 2941; nonflavonoids, 262.6; catechins, 726.6. Anthocyanins were found at 239.7 mg M-3-G/L, and resveratrol was found at 2.00 mg/L. A study of three Argentinean wine varieties found that (a) the TPC content of the Cabernet Sauvignon wine (2300 mg/L GAE) was lower than those of Malbec (2522 mg/L GAE) and Merlot (2704 mg/L GAE) varieties; (b) the relative antimicrobial activities against E. coli and L. monocytogenes in a meat model treated with 100 and 200 mg/L of isolated

different wine varieties. For example, the analysis of 67 Italian wines showed that red wines contained 19.3 mg/L total biogenic amines, rose wines, 9.2 mg/L, and white wines, 7.67 mg/L, with histamine, tyramine, and cadaverine as the most representative amines.102 Catecholamines. Bioactive compounds from wines and other foods can occasionally inhibit cytosolic sulfotransferases (SULTs) that catalyze the sulfonation (metabolism) of catecholamines (dopamine, epinephrine), resulting in increased plasma levels of these bioactive compounds that can trigger migraine headache, increased blood pressure, and atrial fibrillation.103 D-Amino Acids. Low levels of D-amino acids (D-Ala, D-Glu, and D-Lys) are produced by Saccharomyces cerevisiae and Oenococcus oeni during fermentation of wine.104 Another study105 found that the concentrations of D-amino amino acids relative to the corresponding L-enantiomers ranged for white wines from 0.4 to 3.9% D-Ala, from 0.9 to 8.3% D-Asx, and from 0.5 to 8.9% D-Glx; in red wines, from 2.9 to 10.6% DAla, from 2.2 to 10.9% D-Asx, and from 3.9 to 7.4% D-Glx. Storage times of bottled wines up to 24 years did not correlate with D-amino acid content. Studies on the nutrition and safety of D-amino acids reported that D-Lys is not bioavailable as a source of L-Lys and that certain D-amino amino acids inhibited the growth of mice.106,107 Homocysteine. Analysis of 32 different wines showed that the average homocysteine content, an amino acid that is linked to cardiovascular disease106,108 and to macular edema and neuropathy in patients with type 2 diabetes,109 was 10.31 and 6.11 μM and in red and white wines, respectively.110 Ochratoxin A. The possible human carcinogen ochratoxin A produced by Aspergillus and Penicillium fungal species111 was found to be present in about 50% of all evaluated wines at levels that are generally lower than the European Union (EU) regulatory level of 2 μg/L.112−117 Sulfites. Sulfites added to wines as antimicrobial preservatives to extend shelf life may aggravate symptoms of allergic asthma.8,118,119 Wine labels suggest that susceptible individuals need to be aware of the possible adverse effects of wines. With the above brief overview of wine composition, sensory properties, bioactivities, and possible adverse effects as background, reported studies on the antimicrobial, antiviral, and antifungal potential of wines and wine byproducts, in culture, in vivo, and on/in food will now be described.

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ANTIBACTERIAL PROPERTIES Wines. This section presents brief overviews of reported studies on the growth inhibition of bacteria that can cause human illness. The individual pathogens are listed alphabetically followed by studies that cover multiple pathogens. General comments concerning pathogenicity are based on information listed in a book on foodborne pathogens120 and in The Merck Manual of Diagnosis and Therapy.121 Bacillus cereus. This foodborne pathogen causes vomiting and diarrhea. A study on wine-induced inactivation of B. cereus found that (a) wine inactivated B. cereus cultures to undetectable levels in 21 °C > 4 °C, (b) storage for up to 2 months did not affect activities against Salmonella, (c) combinations of antimicrobials in wine exhibited additive antimicrobial effects, and (d) polyphenolic compounds isolated by chromatography separation from red wine exhibited exceptional activity at nanogram levels against two strains of B. cereus. The cited beneficial effects seem to have stimulated interest in defining the efficacy of wine marinades against contaminated meat products outlined below. The populations of Carnobacterium maltaromaticum, L. monocytogenes, Brochothrix thermosphacta, and C. jejuni bacteria were reduced by ∼1.5, 2, 3, and 6 log CFU, respectively, on contaminated pork meat submerged into Spanish red wine for 15 min followed by storage at 4 °C for 3 days.151 Except for C. maltaromaticum, ultrasound treatment with red wine acted synergistically against the pathogens, suggesting that marinating can be used to enhance the taste, texture, and safety of pork meat counts (7 log CFU/mL) and low counts (3 logs CFU/ mL) of C. jejuni. The bacteria were completely inactivated in both white and red wines. Immersion of poultry meat contaminated with this pathogen in both wine marinades was less effective in reducing the microbial levels.152 Immersion of contaminated beef fillets in Greek red wine or wine supplemented with 0.3% thyme oil for 12 h significantly reduced the levels of acid-adapted and -nonadapted S. enterica Typhimurium compared to nonmarinated control samples by 2.0 and 1.9 log CFU/g, respectively, during storage for 19 days at 5 °C.155 The addition of thyme oil to the wine seems to increase the antimicrobial effect of marinades, suggesting the marinating can be used to extend the shelf life of meats.

phenolic compounds paralleled the phenolic content of the wines; and (c) the polyphenol effect was ethanol-independent, suggesting that phenolic content governs activity and the need to produce new wine varieties with high polyphenolic content.131 Wine Varieties. A study of the antimicrobial effects of three Argentinean wines with different phenolic contents against multiple organisms showed that E. coli was the most sensitive bacterium to Merlot wine and that clarified wines, prepared by exposure of red wines to charcoal to remove phenolic compounds, were inactive.132 A study of the composition and antioxidative and antimicrobial effect of six Serbian wines prepared from different grape varieties against nine different pathogenic bacteria showed that the contents of two wine flavonoids, quercetin and quercetin-3-glucoside, can be used as biochemical markers for antioxidative and antimicrobial bioactivities.133 An evaluation of Moroccan Cabernet Sauvignon, Merlot, and Syrah red wine fractions against four Gram-positive bacteria, nine Gram-negative bacteria, two yeasts, and four molds showed that the Cabernet Sauvignon wine, as well as fractions with the highest monomeric anthocyanin content, were the most active, suggesting that these compounds largely contribute to the antimicrobial effects associated with wine components.34 Winery Byproducts. An analytical and antimicrobial study of the polyphenolic profile of GSEs from seven red and seven white Croatian grape varieties showed that (a) the total phenols, flavonoids, catechins, flavanols, and individual polyphenols [(+)-catechin, (−)-epicatechin, epicatechin gallate, procyanidins B1 and B2, quercetin glucoside, resveratrol monomers, piceid, and astringin] was variety dependent; (b) the TPC (>70 mg/g DM) of red skins of red cultivars were much higher in phenolic content than the skins from white cultivars (>20 mg); (b) antioxidative properties were related to polyphenolic content; (c) the average content of highly bioactive trans-resveratrol of 0.29 mg/kg of fresh berry wt was lower than the corresponding value of 0.59 mg/kg of fresh berry wt in the extracts from the red varieties; (d) the corresponding values for cis-resveratrol were 0.30 and 0.80 mg/ kg of fresh berry wt, respectively; (e) minimum inhibitory concentration (MIC) values against multiple organisms (Grampositive B. cereus and S. aureus and Gram-negative C. jejuni, E. coli, and Salmonella infantis) ranged from 0.014 to 0.59 mg GAE/mL; and (f) MICs of white cultivars against E. coli and Salmonella, the most frequent causes of foodborne infections, were the lowest (highest activity).134 Resveratrol. Although present in small amounts in wine, resveratrol is probably the most widely studied flavonoid.135−137 This phytoalexin phenolic compound is reported to inhibit the growth of microbial species (S. aureus, Enterococcus faecalis, and Pseudomonas aeruginosa) as well as several pathogenic fungal dermatophytes that cause skin infections,138 to inhibit biofilm formation of E. coli O157:H7 and P. aeruginosa,139,140 and V. cholerae,141 to reduce the growth rates of numerous animal-associated bacteria in culture,142 and to exhibit cytotoxicity against T. vaginalis, the cause of the sexually transmitted disease trichomoniasis.143 It seems that resveratrol exhibits antimicrobial, antiparasitic, and antiinflammatory properties that have the potential to benefit microbial food safety and human infections. 4-Hydroxytyrosol. We previously reported that this olive compound inhibited both the growth of foodborne pathogens and the biological activity of a bacterial toxin.111,144,145 Because 6030

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highest activity.167 These results indicate that muscadine juice can be used as an active antimicrobial ingredient against these pathogens in nonalcoholic beverages. A related study by the same investigators168 found that water-soluble muscadine GSE prepared from the purple cultivar Ison and the bronze cultivar Carlos exhibited strong antimicrobial activity against a cocktail of three strains of E. coli O157:H7 and that heat treatment of both extracts increased antimicrobial activity, possibly because of increased acidity, tartaric acid, and individual and total phenolic content. These results suggest that water-soluble muscadine seed extracts could serve as natural preservatives in beverages. Electrostatic spraying of GSE onto contaminated lettuce and spinach samples with GSE alone and in combination with lactic, malic, or tartaric acids reduced E. coli levels on spinach up to 4.0 log CFU/g and on spinach up 2.8 log CFU/g during the 14 day storage, suggesting that electrospraying technology could help lower risks due to pathogen contamination of fresh produce.169 Commercial grape seed and grape pomace extracts inhibited antitoxin properties of the Shiga toxins Stx1 and Stx2 produced by E. coli O157:H7 bacteria.170 Because red and white wines and phenolic compounds isolated by chromatography from red wine exhibited strong antimicrobial activities against E. coli and other pathogens,123 it would be of interest to find out whether the wine compounds can concurrently or consecutively inactivate the foodborne pathogens and the toxins produced by the pathogens. We previously reviewed the inactivation of food-related microbial, fungal, and plant toxins by natural compounds.111,123,144 Helicobacter pylori. H. pylori, a Gram-negative organism that has adapted to thrive in the acid conditions of the digestive tract, causes gastritis, peptic ulcers, and adenocarcinoma. To help overcome multidrug resistance, Brown et al.171 evaluated the efficacy of muscadine grape skin and two polyphenolic constituents against H. pylori. They found that (a) grape skin and quercetin inhibited H. pylori infection in mice; (b) quercetin and resveratrol reduced the bacterial counts of the pathogen with MIC values of 256 and 128 μg/mL, respectively; (c) grape skin extracts were more effective than the two constituents; and (d) the inhibitions were dose dependent and pH independent.172 The observed anti-H. pylori effects suggest that the extracts and components might be used in a diet-based approach for the prevention and/or treatment of H. pylori infection. A related study found that a comparison of the inhibition of H. pylori by grape seed, skin, and seed plus skin extracts of two grape varieties showed that the highest observed zone of inhibition was with the seed extracts, with MIC and minimum bactericidal concentration (BMC) values of 2048 μg/ mL of the extracts of both varieties.172,173 Klebsiella pneumoniae. K. pneumoniae causes lung and urinary infections that occur mainly in hospital patients with diminished resistance. Because some isolates are resistant to medical antibiotics, there is a need for new antimicrobials to overcome infections associated with this pathogen. Ethanol extracts of grape seeds were found to be more effective in inhibiting K. pneumoniae than were grape skin extracts, suggesting a potential value for the seed extract against human infections.174 These authors also found that the seed extract was also active against E. faecalis and E. coli. Listeria monocytogenes. L. monocytogenes is a Grampositive foodborne bacterial pathogen that causes human listeriosis, with symptoms ranging from headaches to

Greek red wine with and without 0.5% oregano oil induced reduced levels of S. enterica and L. monocytogenes on contaminated beef pieces after storage at 5 °C for 18 h by 2.1 and 3.4 log CFU/cm2.156 Because the addition of oregano oil enhanced the antimicrobial activity and no changes in heat resistance were apparent during storage of the beef samples, wine marinating can enhance both safety and shelf life. Marinating with soy sauce or red wine marinades can control oxidation and microbial spoilage of raw beef, suggesting that marinating can extend the shelf life of meat.158 A wine-based marinade with added garlic powder or juice and a starter culture of Lactobacillus sakei induced loss of viability of L. monocytogenes and Salmonella spp. in a Portuguese dry sausage made from wine-marinated pork.156 A related study optimized the drying conditions to protect the sausage against Salmonella, Listeria, and S. aureus.159 As described in detail elsewhere, there is a need to reduce both pathogens and heat-induced potentially carcinogenic heterocyclic amines in cooked meat products.160,161 Wine marinades without and with added herbs used as meat flavoring (garlic, ginger, thyme, rosemary, and red chilli peppers) reduced the formation of heterocyclic amines in pan-fried beef.162 Additional studies found no correlation between the marinade-induced antioxidant activities and individual or total heterocyclic amine formation.162 Related studies on the reduction of amine formation by wine-fried chicken breast are described by Brusquest et al.163 The concurrent reduction of both pathogens and heterocyclic amines by wine marinades with added herbs merits study. Brannan found that 0.1% GSE inhibited the intensity of musty and rancid odor and rancid flavor, but caused color darkening, on ground chicken breast and thigh during refrigerated storage, suggesting that the seed extract may be an effective antioxidant in precooked chicken products.164 Grape Seed Extracts. This section presents brief overviews of reported studies on the inhibition of growth and/or destruction of pathogenic microorganisms by GSEs. Brochothrix thermofacta. GSE incorporated into pea starch films with pork loins infected with the psychotrophic spoilage organism B. thermofacta reduced the bacterial growth on surface-inoculated pork loins by 1.3 log CFU/mL after 4 days of incubation at 4 °C.20 Additional studies showed that GSE films also inhibited the growth of the following pathogens: S. aureus, E. faecalis, E. faecium, and L. monocytogenes. The authors suggest that biodegradable and edible GSE antimicrobial films have the potential to improve meat quality and extend shelf life. Cronobacter sakazakii. C. sakazakii is a Gram-negative, anaerobic bacterium of the family Enterobacteriaceae reported to cause infection in adults and children, especially infants.165 Freshly prepared red muscadine grape juices induced a 6 log reduction of C. sakazakii after a 2 h incubation at 37 °C, suggesting that red muscadine juice could inhibit the pathogen in baby food.166 Escherichia coli O157:H7. E. coli O157:H7 is a foodborne, toxin-producing enteropathogen responsible for hemorrhagic colitis, bloody diarrhea, and hemolytic uremic syndrome. Here, we will briefly review reported activities of grape-derived products against this organism. A study on the effect of fresh and processed muscadine red grape juices against a 5 log cocktail of cells of E. coli O157:H7 incubated for 4 h at 37 °C showed that polar fractions containing malic, tartaric, and tannic acids showed strong antimicrobial activity and that synthetic tannic acid showed the 6031



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monocytogenes in vacuum-marinated irradiated chicken breast meat without affecting consumer acceptance of the product, suggesting that the combination of the plant formulations with levels of irradiation below the maximum allowed could contribute to the prevention of contamination by Listeria.183 Chitosan films impregnated with GSE inhibited L. monocytogenes as well as aerobic mesophiles and lactic acid bacteria on sausages during refrigerated storage, suggesting that the antimicrobial chitosan films could extend the shelf life of sausages.184,185 Maximum growth inhibition (∼2.0 log CFU/g) of L. monocytogenes was observed in chicken and turkey hot dogs treated with combinations of potassium lactate and sodium diacetate with green tea and grape seed extracts. The antilisterial effect was enhanced by heat treatment of the hot dogs, suggesting that the extracts can partially replace the chemical preservatives and enhance the antilisterial activities.186 Staphylococcus aureus. S. aureus is a Gram-positive, aerobic, toxin-producing foodborne pathogen that can also contaminate the skin, lung, heart, and other organs. A total ethanol grape extract prepared by the percolation method of whole grapes inhibited S. aureus, suggesting that the extract represents a natural antibacterial for possible treatment of local skin infections.187 Pomace, seed, and skin extracts from New Zealand Pinot noir grapes were more effective against S. aureus bacteria than extracts from Pinot Meunier grapes, suggesting that extraction solvent, fraction, and grape variety significantly influence antimicrobial properties. A weak but significant relationship was observed between TPC and antimicrobial effects (r = 0.58).17 A screening assay showed that bioactive polyphenols from pomace concentrated onto a protein-rich matrix inhibited the proliferation of S. aureus bacteria on the skin.188 Vibrio cholerae. V. cholerae produces a cholera toxin that causes watery diarrhea of cholera, an often fatal disease.111 Two grape extracts sold as nutritional supplements inhibited the cholera toxin, as well as the heat-labile Shiga toxin produced by E. coli in cultured cells and intestinal loops by blocking toxin binding to the cell surface.189,190 These results suggest that grape extracts could help ameliorate cholera in humans. Vibrio vulnificus/Vibrio parahemolyticus. V. vulnificus, a Gram-negative foodborne bacterium present in estuarine environments where oysters are harvested, has a 40−50% fatality rate. Dipping of oysters contaminated with V. vulnificus in solutions of GSE (500 mg/mL), citric acid (300 mg/mL), or lactic acid (150 mg/mL) reduced the pathogens to levels lower than control samples during refrigerated storage for 20 days.191 The MIC value of V. parahemolyticus in artificially inoculated oysters dipped in GSE solutions was 10 mg/mL; a solution of 500 mg/mL of GSE reduced the population below detection level.191 Multiple Pathogens. An in vitro study showed that GSE was more effective in inhibiting Gram-positive bacteria (S. aureus, L. innocua, and B. thermosphacta) than Gram-negative ones (E. coli, P. aeruginosa, and S. enterica), suggesting that GSE can inhibit the most frequent causes of foodborne bacterial infections in developed countries.174,192,193 A Turkish study found that GSEs completely inhibited Gram-positive (B. cereus, B. coagulans, B. subtilis, and S. aureus) and, less so, Gramnegative (E. coli and P. aeruginosa) bacteria.194 GSE with a high total phenolic content (628 mg GAE/g) inhibited the growth of the following spoilage and pathogenic bacteria: Aeromonas hydrophila, Bacillus brevis, B. cereus, Bacillus

bacteremia, septicemia, encephalitis, and meningitis and a mortality rate of about 20−30%.175 We now will record efforts to inactivate the pathogen with grape products. Grape juice and skin extracts from black table grapes strongly inhibited multiple L. monocytogenes species but did not inhibit B. cereus, Salmonella Menston, E. coli, S. aureus, or Y. enterocolitica pathogens.176 Fractionation of the extracts showed that the antilisterial activity was highest in the polymeric phenolic fractions, that activity of the red-pigmented fractions was pH dependent, and that the unpigmented polymeric phenolics from the seed showed pH-independent activity. The observed reduction was striking, from ∼log CFU7 to undetectable levels after 10 min. Evidently, both pigmented and unpigmented phenolic compounds from grapes were bioactive against Listeria, but apparently not against the other mentioned pathogens. Chardonnay and black raspberry seed flour extracts at 165 and 160 μg seed flour equivalents/mL inhibited the growth of L. monocytogenes and E. coli with zero survival rates under the test conditions. These results and compositional and antioxidant activities suggest that the seed flours have the potential to serve as natural food preservatives for improving food stability, quality, and safety, and consumer acceptance.177 Dipping of surface-inoculated (log 6 CFU/g) turkey frankfurters into soy protein film-forming solutions without and with antimicrobials (1% GSE plus nisin, 10000 IU/mL) resulted in 2.8 log CFU reduction of L. monocytogenes after storage for 28 days at 4 or 10 °C, suggesting that the antilisterial activity of the combination was greater than that observed with the individual antimicrobials and that the use of antimicrobial films may enhance the microbial safety of meat products.178 Because the combination of antimicrobials caused a much higher 9 log cycle reduction in culture, it seems that antimicrobial results in the absence of food do not predict the efficacy in a meat matrix. Dipping contaminated turkey frankfurters with 1% GSE plus nisin (6400 IU/mL) reduced the L. monocytogenes population from ∼log 7 CFU/g to undetectable levels after storage at 4 or 10 °C for 21 days, suggesting that the combination can improve the antimicrobial efficacy against this pathogen in refrigerated ready-to-eat (RTE) meat and poultry storage.179 A related study180 found that soy protein edible films containing GSE, nisin, and EDTA were more effective in inhibiting the growth of L. monocytogenes (reduction of 2.9 log CFU/mL) than E. coli (1.8 log reduction) or Salmonella Typhimurium (0.6 log reduction), suggesting that the susceptibility of the pathogens to inhibition is not uniform. Dipping turkey frankfurters contaminated with L. monocytogenes, E. coli O157:H7, or Salmonella Typhimurium (∼6 log CFU/g) into a whey protein isolate coating incorporated with GSE (0.5%) and nisin (6000 IU/g) followed by storage for 28 days at 4 °C reduced the bacterial population by 2.3, 4.6, and 1.0 log cycles, respectively, confirming that antimicrobial protein coatings can be used to inhibit foodborne pathogens in meat.181 Grape seed and stem extracts from the red Greek grape variety Mandilaria containing high concentrations of flavan-3ols and derivatives represent a source of potent antilisterial compounds with low MIC values of 0.26−0.34. The extracts have the potential to serve as food additives to prevent the growth of L. monocytogenes.182 The addition of tartaric acid and grape seed and green tea extracts added to chicken marinades significantly reduced L. 6032



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megaterium, Bacillus subtilis, Enterobacter aerogenes, E. faecalis, E. coli, K. pneumoniae, L. monocytogenes, Mycobacterium smegmatis, Proteus vulgaris, P. aeruginosa, and S. aureus.21,22 It seems that GSE with a high polyphenolic content can act as a broadspectrum antibiotic in food contaminated with multiple pathogens. Grape Pomace Extracts. Pomace extracts (5 and 10% concentration) from five Turkish grape varieties inhibited pathogenic (S. aureus, coliforms, Enterobacteriaceae, Enterococci, and Salmonella) as well as spoilage organisms (lactobacilli, lactococci, lipolytic bacteria, Micrococaceae, and proteolytic and psychotrophic bacteria) in beef patties, suggesting that the extracts could serve as antimicrobial agents that can prevent the deterioration of meat products.32,195 Pomaces from Pinot noir and Merlot Oregon grapes with TPC of 21.2−76.7 GAE/g DM, anthocyanin content of 0.35− 0.76 mg Mal-3-glu/g DM, total flavonoid content (TFC) of 30.2−106.1 mg CE/g DM, and dietary fiber content of 57− 63% of total dry matter (DM) showed higher activity against L. innocua than against E. coli.196 The pomace extracts were more active against the bacteria than the skin extracts. All samples lost significant amounts of bioactive compounds during 16 weeks of storage, with freeze-dried samples retaining higher amounts of TPC than samples stored at ambient temperatures or 40 °C. The authors suggest that the two pomaces could be used as functional food ingredients that can promote human health. An evaluation of the antimicrobial efficacy of grape pomace powder and pomace extracts from Turkish grape varieties showed that a 10% concentration of the powder completely inhibited S. aureus in vegetable soup at the end of 120 h and that this pathogen was more susceptible to inhibition than E. coli.197 The same authors also analyzed the data by an adaptive neuro fuzzy inference system (ANFIS), an artificial neural network (ANN), and multiple linear regression (MLR) models to predict antibacterial effects of the two pathogens in the soup. Supercritical fluid pomace extracts from Brazilian grapes were more effective against Gram-positive bacteria (S. aureus and B. cereus) than against Gram-negative ones (P. aeruginosa and E. coli).41 Seed and skin extracts from grape winery byproducts of the Portuguese Arinto variety showed higher antimicrobial activity against five bacteria and yeast species (E. coli, Salmonella Poona, B. cereus, S. cerevisiae, and C. albicans) than did some of the individual components, suggesting that the extracts can both protect against the adverse effects of contaminated food and be used to prevent or treat animal and human infectious diseases.198 Pomace extract-based polysaccharide films induced ∼5 log reduction in bacterial activity against E. coli and up to a 3.0 log reduction against L. innocua on a Petri dish at the end of a 24 h test compared to the control, suggesting the need to evaluate the films for applicability to contaminated food.20,199 We evaluated the relative bactericidal activities of 10 presumed health-promoting food-based powders (neutraceuticals) and, for comparison, selected known components against the following foodborne pathogens: E. coli O157:H7, S. enterica, L. monocytogenes, and S. aureus.144 The relative activities were evaluated using quantitative bactericidal activity (BA50 value, defined as the percentage of the sample in the assay mixture that resulted in a 50% decrease in colony-forming units). The BA50 values were determined by fitting the data to a sigmoidal curve by regression analysis using concentration−antimicrobial response data. Antimicrobial activity is indicated by a low BA50

value, meaning less material is needed to kill 50% of the bacteria. Olive pomace, olive juice powder, and oregano leaves were active against all four pathogens, suggesting that they behave as broad-spectrum antimicrobials. All powders exhibited strong antimicrobial activity against S. aureus. The following powders showed exceptionally high activity against S. aureus (as indicated by the low BA50 values shown in parentheses): apple skin extract (0.002%); olive pomace (0.008%); and GSE (0.016%). Listeria bacteria were also highly susceptible to apple skin extract (0.007%). The most active substances provide candidates for the evaluation of antimicrobial effectiveness in human foods and animal feeds.

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ORAL PATHOGENIC BACTERIA Several studies describe anticariogenic/cariostatic effects of grape products. These include the following observations. Phenolic extracts with highly variable anthocyanin and flavan-3ol contents prepared from several red wine grape varieties and their fermented byproduct of winemaking (pomace) were highly effective against virulence traits of the dental pathogen Streptococcus mutans, suggesting their potential value against dental disease.200−204 A study on bacterial adherence to enamel in the oral cavity of six human subjects revealed that rinses with red wine and teas induced up to a 66% reduction of adherent bacteria compared to controls, suggesting that these beverages might contribute to the prevention of biofilm-induced diseases in the oral cavity.205 A red wine GSE reduced plaque area on bovine teeth in an artificial mouth by 40% compared to the control. This value was, however, lower than corresponding reductions of 84.0 and 87.5%, respectively, observed with Salvia officinalis and Rosmarinus officinalis plant extracts.206 An evaluation of the antibacterial activities of wine phenolic compounds and GSEs against potential respiratory pathogens present in the oral cavity that contribute to the formation of dental plaque showed that (a) gallic acid and ethyl gallate had the highest activity, (b) two commercial GSEs were more active than the phenolic compounds, and (c) Gram-positive bacteria (E. faecalis, S. aureus, and Streptococcus pneumoniae) were more susceptible to inactivation than Gram-negative bacteria (Moraxella catarrhalis and P. aerations).207 Red wine alone and with added GSE inhibited oral microbiota in a five-species biofilm model of supragingival plaque.208 These observations suggest the need to evaluate the germ-killing efficacy of wine compounds in oral rinses and chewing gums.

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ANTIVIRAL ACTIVITIES Viral contamination of food and infection of animals and humans is a major cause of numerous diseases. The mechanism of antiviral action of plant polyphenolic compounds is based on their abilities to act as antioxidants, to inhibit essential enzymes, to disrupt cell membranes, to prevent viral binding and penetration into cells, and to trigger the host cell self-defense mechanism.209 Here, we present a brief overview of reported studies on the antiviral activities of grape products against pathogenic viruses. Adenovirus. A polyphenol-based grape extract from Portuguese white-winemaking byproducts and resveratrol reduced adenovirus-5 production by 4.5 and 6.5 log (TCID50/mL). In contrast to resveratrol, the extract irreversibly inhibited the replication of the adenovirus, suggesting its potential value as an antiviral agent.210 6033



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Cytomegalovirus. The wine polyphenolic compound resveratrol reduced human cytomegalovirus DNA replication to undetectable levels by blockage of epidermal growth factor receptor activation in human embryonic fibroblasts.211 Hepatitis Viruses and Virus Surrogates. A study of the effect of commercial GSE on human enteric virus surrogates and hepatitis A virus evaluated the infectivity of the virus exposed to GSE concentrations of 0.5, 1, and 2 mg/mL for 2 h at room temperature or 37 °C.212,213 At high titer (∼log 7 PFU/mL), the infectivity was reduced by up to 4.61 log PFU in a dose-dependent manner, suggesting that GSE has the potential to be used by the food industry as an inexpensive novel natural broad-spectrum antiviral alternative to reduce viral contamination and enhance food safety and quality. Noroviruses. The foodborne norovirus causes gastroenteritis and diarrhea in humans. An examination of the effect of GSE against the human norovirus by a plaque and other bioassays for murine norovirus found that GSE at 0.2 and 2 mg/mL reduced the infectivity by >3 log PFU/mL of the murine virus and the binding of the human norovirus to salivary human histo-blood group antigen receptors.213−215 The observed 1.5−2 log PFU/mL reduction in the murine virus titer following addition of 2 mg of GSE/mL to sanitized water in the washing bath of fresh-cut lettuce suggests the potential value of the treatment to reduce the viral burden of leafy greens. The mechanism of the antiviral effect seems to involve denaturation of the viral capsid protein. GSE was also effective against these viruses on contaminated produce.215 Thus, treatment of lettuce and jalapeno peppers (25−30 g) inoculated with human norovirus surrogates (feline calicivirus and murine norovirus) or hepatitis A virus with 0.25, 0.5, 1 mg/mL GSE or water for 30 s−5 min reduced the viral counts from ∼7 log PFU/mL to 2.33, 2.58, and 2.71 log PFU on lettuce and to 2.20, 2.74, and 3.05 log PFU on peppers after 1 min at all three concentrations, respectively. The authors suggest that GSE should be considered for use as part of hurdle approaches that combine GSE with other antiviral treatments for foodborne virus reduction on produce. Rotaviruses. Exposure of rotaviruses, the most common cause of severe diarrhea in children, to grape and cranberry juices and proanthocyanidins resulted in a loss of viral infectivity after 5 min via blockage of viral antigenic determinants caused by modification of viral integrity at physiological pH, suggesting that the fruit juices may help protect against viral-induced diarrheas.216,217 A related study by Ko et al.218 reported that an orally administered alcohol-free Cabernet Sauvignon red wine extract inhibited diarrhea in a neonatal mouse model of rotaviral infection, but did not prevent watery stools in the mice administered cholera toxin.219,220 Nair et al.221 found that the flavonoid constituents of GSE seem to exert antiviral effects by inducing Th1-derived cytokine γ-interferon (IFN-γ) by peripheral mononuclear cells, suggesting that the beneficial immunostimulatory effect of GSE may be mediated through induction of IFN-γ.222

overcome this problem. Related studies reported that pomaces from other grape varieties inhibited the growth of Zygosaccharomyces rouxii and Zygosaccharomyces bailii32,195 and that GPE from three Chilean grape varieties showed a large inhibitory effect on mycelia growth of B. cinerea with an IC50 value of 50 ppm.30,35 Candida albicans and Other Human Fungal Pathogens. GPE from Brazilian Merlot grapes exhibited moderate activity against three fungal species (C. albicans, Candida krusei, and Candida parapsilosis), with MIC values ranging from 500 to 1000 μg/mL.41 GSE acted synergistically with the medicinal antibiotic amphotericin B against C. albicans, the most common cause of fungal disease in humans, suggesting that the combination with 75% less antibiotic merits use in human fungal infections.223−225 The authors suggest that synergism of natural compounds such as GSE with medicinal antibiotics has the potential to benefit the fight against human infectious diseases. Phenolic red and white wine extracts also inhibit C. albicans.226

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MISCELLANEOUS ASPECTS Anticoccidiosis Activity. GSE from grapes and other plant extracts significantly decreased adverse effects in broiler chickens infected with the parasitic organisms (E. tenella, E. maxima, and E. acervulina) that cause coccidiosis, a poultry disease that results in large economic losses.227,228 The protection involved decreased mortality and improved feed conversion ratio (FCR), suggesting that antioxidant-containing plant extracts may be of benefit in the management of coccidiosis. A related study reported that a 0.1% GSE inhibited the intensity of musty and rancid odor and rancid flavor in chicken breast compared with control patties, suggesting that the extract may be an effective antioxidant in precooked chicken breast.164,229 Caenorhabditis elegans. Pomace flavanols and flavonols (122.75 and 23.11 mg/100 g dry pomace) from Zalema grapes seem to be responsible for the increased survival of C. elegans worms exposed to thermally induced oxidative stress.230

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RESEARCH NEEDS AND OUTLOOK In addition to the research needs mentioned earlier, future studies need to address the following food and medical aspects of the properties of wines and wine flavonoids. In this context the term “flavonoid” represents wines, grape pomace, seed, and skin extracts and their flavonoids. • Determine whether the antibiotic activities of flavonoids and wines in vitro can be duplicated in vivo, especially in humans. • Determine the relationship between wine consumption and lower risk of infection in humans. Will frequent consumption of red wine or flavonoids protect against infection and/or ameliorate the severity of infectious disease in humans? • Determine how bioactivities of flavonoids vary, depending on whether they are tested or consumed in the free state or as part of a mixture or a food. • Determine whether flavonoid metabolites formed after absorption into the circulation by animals and humans possess antimicrobial properties. • Define additive or synergistic effects of mixtures of wine flavonoids with other plant antimicrobials, including plant essential oils, apple, and olive compounds, and

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ANTIFUNGAL EFFECTS Botrytis cinerea and Other Phytopathogens. GPE fractions extracted with methanol or ethanol from a mixture of Chilean grape varieties exhibited in vitro antifungal activity against the phytopathogenic fungus B. cinerea that damages grapevines, resulting in extensive economic losses, suggesting that the pomace can provide a low-cost fungicide to help 6034



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ABBREVIATIONS USED ANFIS, adaptive neuro fuzzy inference system; ANN, artificial neural network; BA50, percent of sample that resulted in a 50% decrease in CFU; CE, catechin equivalents; CFU, colonyforming units; DAD, diode array detector; DM, dry matter; FCR, feed conversion ratio; IC50, analogous to BA50; GAE, gallic acid equivalent; GPE, grape pomace extract; GRAS, generally accepted as safe; GSE, grape seed extract; GSH, reduced glutathione; MIC, minimum inhibitory concentration; MLR, multiple linear regression; IFN-γ, γ-interferon; ROS, reactive oxygen species; SULTs, cytostolic sulfotransfrases; RTE, ready-to-eat; TCID50, tissue concentration infectious dose 50%; TEAC, trolox equivalent antioxidant capacity; TFC, total flavonoid content; Th1, type 1 helper T cells; TPC, total phenolic content

seashell-derived chitosans. Combinations of food ingredients that act synergistically will lessen amounts needed to design effective antimicrobial food formulations. They will be safer and affect flavor and taste less than individual compounds. • Evaluate the effectiveness of wines and flavonoids against antibiotic resistant foodborne and medical pathogens, a largely unexplored area.231−234 • Determine whether flavonoids can additively or synergistically enhance antibiotic properties of medicinal antibiotics. • Determine whether wine flavonoids can protect against bacterial infection through stimulation of the immune system.88,89,235 • Determine antibacterial, antiviral, antifungal, and antitoxin efficacies of wines and flavonoids in various contaminated foods including leafy greens, fruits and fruit juices, vegetables, dairy, meat, poultry, and seafood products. • Develop methods to simultaneously reduce both pathogens and carcinogenic heterocyclic amine levels in processed meat products. • Develop flavonoid-containing edible antimicrobial films and coatings to protect food against contamination by pathogens. • Determine whether flavonoids can prevent biofilm formation by bacteria on contaminated food. • Determine whether the flavonoid content of wines and byproducts can predict antibiotic activities. • Determine whether molecular modeling of flavonoid structure−cell membrane interactions can be used to explain the antibiotic mechanisms of structurally different flavonoids.236−238 • Encourage growers to produce grapes with a high content of bioactive compounds. In summary, because grape phenolic phytonutrients are considered to be generally accepted as safe, the cited and proposed studies will provide numerous benefits. The most active compounds could be used to protect liquid and solid foods against contamination by pathogenic and spoilage microorganisms and microbial toxins as well as therapeutically to treat animal and human infections. The grape pomace, seed, and skin extracts have the potential to provide inexpensive sources of compounds for use against a broad range of diseases. These byproducts will also provide a source of income to grape growers and wine producers. Growers will be encouraged to produce grapes with high levels of bioactive compounds.

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REFERENCES

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS I am most grateful to Carol E. Levin for assistance with the preparation of the manuscript, to colleagues for excellent scientific collaboration, and to journal reviewers for constructive comments. 6035



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Trichomonas vaginalis. Antimicrob. Agents Chemother. 2013, 57, 2476− 2484. (144) 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. (145) Brenes, M.; Medina, E.; García, A.; Romero, C.; De Castro, A. Olives and olive oil compounds active against pathogenic microorganisms. In Olives and Olive Oil in Health and Disease Prevention; Elsevier: Amsterdam, The Netherlands, 2010; pp 1013−1019. (146) Piñeiro, Z.; Cantos-Villar, E.; Palma, M.; Puertas, B. Direct liquid chromatography method for the simultaneous quantification of hydroxytyrosol and tyrosol in red wines. J. Agric. Food Chem. 2011, 59, 11683−11689. (147) Fernández-Mar, M. I.; Mateos, R.; García-Parrilla, M. C.; Puertas, B.; Cantos-Villar, E. Bioactive compounds in wine: resveratrol, hydroxytyrosol and melatonin: a review. Food Chem. 2012, 130, 797− 813. (148) Queipo-Ortuño, M. I.; Boto-Ordóñez, M.; Murri, M.; GomezZumaquero, J. M.; Clemente-Postigo, M.; Estruch, R.; Cardona Diaz, F.; Andrés-Lacueva, C.; Tinahones, F. J. Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers. Am. J. Clin. Nutr. 2012, 95, 1323−1334. (149) Jiménez, A.; Sánchez-González, L.; Desobry, S.; Chiralt, A.; Tehrany, E. A. Influence of nanoliposomes incorporation on properties of film forming dispersions and films based on corn starch and sodium caseinate. Food Hydrocolloids 2014, 35, 159−169. (150) Melo, A.; Viegas, O.; Petisca, C.; Pinho, O.; Ferreira, I. M. P. L. V. Effect of beer/red wine marinades on the formation of heterocyclic aromatic amines in pan-fried beef. J. Agric. Food Chem. 2008, 56, 10625−10632. (151) Birk, T.; Knøchel, S. Fate of food-associated bacteria in pork as affected by marinade, temperature, and ultrasound. J. Food Prot. 2009, 72, 549−555. (152) Isohanni, P.; Alter, T.; Saris, P.; Lyhs, U. Wines as possible meat marinade ingredients possess antimicrobial potential against Campylobacter. Poult. Sci. 2010, 89, 2704−2710. (153) Istrati, D.; Ionescu, A.; Vizireanu, C.; Ciuciu, A. M. S.; Dinica, R. The tenderization of bovine Biceps femoris muscle using marinades on the basis of wine. Rom. Biotechnol. Lett. 2012, 17, 7787−7795. (154) Linares, M. B.; Garrido, M. D.; Martins, C.; Patarata, L. Efficacies of garlic and L. sakei in wine-based marinades for controlling Listeria monocytogenes and Salmonella spp. in chouriço de vinho, a dry sausage made from wine-marinated pork. J. Food Sci. 2013, 78, M719− M724. (155) Nisiotou, A.; Chorianopoulos, N. G.; Gounadaki, A.; Panagou, E. Z.; Nychas, G. J. Effect of wine-based marinades on the behavior of Salmonella Typhimurium and background flora in beef fillets. Int. J. Food Microbiol. 2013, 164, 119−127. (156) Rhoades, J.; Kargiotou, C.; Katsanidis, E.; Koutsoumanis, K. P. Use of marination for controlling Salmonella enterica and Listeria monocytogenes in raw beef. Food Microbiol. 2013, 36, 248−253. (157) Friedman, M.; Henika, P. R.; Levin, C. E.; Mandrell, R. E. Recipes for antimicrobial wine marinades against Bacillus cereus, Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella enterica. J. Food Sci. 2007, 72, M207−M213. (158) Kargiotou, C.; Katsanidis, E.; Rhoades, J.; Kontominas, M.; Koutsoumanis, K. Efficacies of soy sauce and wine base marinades for controlling spoilage of raw beef. Food Microbiol. 2011, 28, 158−163. (159) Díez, J. G.; Patarata, L. Behavior of Salmonella spp., Listeria monocytogenes, and Staphylococcus aureus in Chouriço de Vinho, a dry fermented sausage made from wine-marinated meat. J. Food Prot. 2013, 76, 588−594. (160) Friedman, M.; Zhu, L.; Feinstein, Y.; Ravishankar, S. Carvacrol facilitates heat-induced inactivation of Escherichia coli O157:H7 and inhibits formation of heterocyclic amines in grilled ground beef patties. J. Agric. Food Chem. 2009, 57, 1848−1853. (161) Rounds, L.; Havens, C. M.; Feinstein, Y.; Friedman, M.; Ravishankar, S. Plant extracts, spices, and essential oils inactivate

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