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Inhibition of Oral Pathogens Adhesion to Human Gingival Fibroblasts by Wine Polyphenols Alone and in Combination with an Oral Probiotic

  • Adelaida Esteban-Fernández
    Adelaida Esteban-Fernández
    Instituto de Investigación en Ciencias de la Alimentación (CIAL), CSIC-UAM, c/Nicolás Cabrera, 9, 28049 Madrid, Spain
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    • , 
  • Irene Zorraquín-Peña
    Irene Zorraquín-Peña
    Instituto de Investigación en Ciencias de la Alimentación (CIAL), CSIC-UAM, c/Nicolás Cabrera, 9, 28049 Madrid, Spain
    More by Irene Zorraquín-Peña
    • , 
  • Maria D. Ferrer
    Maria D. Ferrer
    Department of Health and Genomics, Center for Advanced Research in Public Health, FISABIO Foundation, 46020 Valencia, Spain
    CIBER Epidemiology and Public Health, 28029 Madrid, Spain
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    • , 
  • Alex Mira
    Alex Mira
    Department of Health and Genomics, Center for Advanced Research in Public Health, FISABIO Foundation, 46020 Valencia, Spain
    CIBER Epidemiology and Public Health, 28029 Madrid, Spain
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    • , 
  • Begoña Bartolomé
    Begoña Bartolomé
    Instituto de Investigación en Ciencias de la Alimentación (CIAL), CSIC-UAM, c/Nicolás Cabrera, 9, 28049 Madrid, Spain
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    • , 
  • Dolores González de Llano
    Dolores González de Llano
    Instituto de Investigación en Ciencias de la Alimentación (CIAL), CSIC-UAM, c/Nicolás Cabrera, 9, 28049 Madrid, Spain
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    • , and 
  • M. Victoria Moreno-Arribas*
    M. Victoria Moreno-Arribas
    Instituto de Investigación en Ciencias de la Alimentación (CIAL), CSIC-UAM, c/Nicolás Cabrera, 9, 28049 Madrid, Spain
    *E-mail: [email protected]
    More by M. Victoria Moreno-Arribas
    Orcidhttp://orcid.org/0000-0002-4136-595X
Cite this: J. Agric. Food Chem. 2018, 66, 9, 2071–2082
Publication Date (Web):February 21, 2018
https://doi.org/10.1021/acs.jafc.7b05466
Copyright © 2018 American Chemical Society
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Abstract

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Several benefits have been described for red wine polyphenols and probiotic strains in the promotion of colonic metabolism and health. On the contrary, knowledge about their role in the management of oral health is still scarce. In this work, the antiadhesive capacity of selected red wine polyphenols and oenological extracts against the oral pathogens Porphyromonas gingivalis, Fusobacterium nucleatum, and Streptococcus mutans in an in vitro model of human gingival fibroblasts has been explored as well as their complementary action with the candidate oral probiotic Streptococcus dentisani. Results highlighted the antiadhesive capacity of caffeic and p-coumaric acids as well as grape seed and red wine oenological extracts. Both, caffeic and p-coumaric acids increased their inhibition potential against S. mutans adhesion when combined with S. dentisani. Additionally, UHPLC–MS/MS analysis demonstrated the oral metabolism of wine phenolics due to both, cellular and bacterial activity.

KEYWORDS:

Introduction

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Polyphenols are defense secondary metabolites found in numerous plant species and their fruits. Their antioxidant activity has been widely studied; however, other beneficial properties have been described for polyphenol-rich food, including promotion of cardiovascular health, protective effect in neurodegenerative disorders, and metabolic diseases prevention. (1) Red wine is a rich source of dietary polyphenols which possesses a unique combination of phenolic structures (mainly flavonoids but also nonflavonoids). (2) Several intervention studies in humans and animals have provided further evidence of the protective effects of moderate wine consumption (∼250 mL per day), on cardiovascular diseases, diabetes, and neurodegenerative disorders as well as in promotion of gut health among others. (2−4) Phenolic components in wine may also have an effect on human microbiota. In particular, different studies have recently shown that red wine consumption can significantly modulate the growth of selected bacteria of colonic microbiota in healthy humans. (5−7)
Oral microbiota is characterized by a high variability and abundance, containing more than 700 species. (8) Most oral bacteria are located in dental plaque, in a biofilm structure attached to hard and soft tissues, (9) due to the production of microbial exopolysaccharides (EPSs). Therefore, attachment to buccal surfaces is a key step on the development of microbial-derived oral pathologies and it takes place in two steps: first, initial surface attachment by primary colonizers (usually streptococci), which originates a microbial monolayer; then, migration of these colonizers and addition of secondary and late colonizers (i.e., Fusobacterium nucleatum, Porphyromonas. gingivalis), (10) which leads to the formation of a multilayered matrix. However, the oral cavity is a dynamic open system which can easily change. Environmental stimuli (i.e., host susceptibility, poor oral hygiene or dietary habits) can modify oral microbiota, altering the natural balance between commensal and pathogenic microorganisms. This imbalance could be translated into an overgrowth of pathogenic population on detriment of commensal microbes, resulting in a shift of microbial ecology and subsequent development of microbial origin oral diseases. (10) Among them, caries and periodontal diseases (periodontitis and gingivitis) can be distinguished. Caries disease results on the dissolution of the tooth enamel due to excessive organic acids production (low pH conditions) by pathogenic bacteria, such as Streptococcus mutans and Streptococcus. sobrinus, considered as starters of the lesion. (11) On the other hand, periodontal diseases are characterized by an increase of Gram-negative species (i.e., P. gingivalis, Campylobacter spp., Treponema denticola, among others) which produce endotoxins which trigger processes of tissue damage, bleeding, inflammation, irritation and, finally, gum detachment. (12) Furthermore, these pathogens are able to display structural moieties that are recognized by host receptors, triggering inflammatory signaling pathways and exacerbated cytokine production. (10) If S. mutans plays an essential role as initiator on caries disease, P. gingivalis is typically found on chronic periodontitis and has been proposed as the “keystone” microbe in periodontitis initiation, whereas F. nucleatum has been mostly described in gingivitis lesions. (10,13)
Traditional therapies used for the maintenance of oral health present some limitations, and the search of natural-origin therapies is gaining attention. In this regard, benefits of polyphenols as new strategies in the prevention and treatment of microbial derived oral pathologies have been widely described. (10) The main action mechanisms of polyphenols against oral microbial diseases include antiadhesive, antimicrobial, or anti-inflammatory activity as well as inhibition of the expression of proteins responsible of bacterial invasiveness. (10)
The use of probiotics in oral health is limited, and most of them are bifidobacteria and lactobacilli, whose natural niche is the gut, (14) which makes it difficult for a successful colonization of the oral cavity. Despite this, the use of probiotics as preventive agents in microbial-derived oral diseases is gaining attention, (15) and some discoveries have pointed out Streptococcus strains as potential candidate probiotics in this field. (16) Concretely, Streptococcus dentisani 7746 has been isolated from dental plaque of caries-free individuals, and the last evidence (14) has demonstrated that this probiotic expresses bacteriocins against the major oral pathogens, including S. mutans, Prevotella intermedia, and F. nucleatum. In addition, other beneficial mechanisms of action have been described for this novel isolate, such as buffering ability in acidogenic biofilms in the presence of arginine, a component of some tooth pastes. (14)
Most bacterial phenolic metabolism takes places in the gut, where microbiota transform polyphenols into simple phenols, lactones, and phenolic and aromatic acids, (17) which are believed to be the real executors of the benefits associated with these bioactive molecules. However, this metabolism starts in the oral cavity due to salivary enzymatic action, chewing, and oral microbiota activity. (2) Despite some evidence describing a degradation of red wine and grape seed extracts flavan-3-ols by pathogenic oral biofilm, (18) knowledge about the role of oral components in phenolic metabolism is still preliminary.
In this context, the effect of selected wine phenolic compounds (caffeic and p-coumaric acids), and red wine and grape seed extracts (Provinols and Vitaflavan, respectively) on F. nucleatum, S. mutans, and P. gingivalis adherence to HGF-1 human fibroblasts has been studied. Furthermore, a possible complementary effect between polyphenols and the candidate oral probiotic S. dentisani 7746 with anticariogenic ability was explored. Finally, the role of oral bacteria and cells to metabolize polyphenols with the subsequent release of phenolic metabolites has been determined.

Materials and Methods

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Wine Extracts and Compounds

Two oenological phenolic extracts (Vitaflavan and Provinols) and two pure phenolic metabolites, caffeic acid (Sigma-Aldrich) and p-coumaric acid (Extrasynthese, France), were used in this study. Vitaflavan, kindly provided by Dr. Piriou (Dérives Resinique & Terpéniques, S.A., France), is a commercial phenolic extract from grape seeds with a total phenolic content of 629 mg of gallic acid equivalents per g. Provinols, kindly supplied by Safic-Alcan Especialidades S.A.U. (Barcelona, Spain) is a red wine extract with a total phenolic content of 474 mg of gallic acid equivalents per g. The phenolic compositions of both extracts were previously determined by UHPLC–ESI-MS/MS (Table 1) (19,20) for other studies. The same batches of both oenological extracts in the papers referred to in Table 1 were employed. So, the concentrations in Table 1 have been assumed from these analyses and are considered as approximated values.
Table 1. Phenolic Characterization (mg/g) of Provinols (Red Wine Extract) and Vitaflavan (Grape Seed Extract), As Previously Determined by UHPLC–ESI-MS/MS (19,20)
flavan-3-ols and othersProvinolsVitaflavana
gallic acid1.06 ± 0.059.11 ± 0.01
catechin9.90 ± 0.3274.6 ± 0.09
epicatechin6.87 ± 0.1567.7 ± 0.75
epicatechin-3-O-gallate0.226 ± 0.01826.2 ± 0.41
procyanidin B111.1 ± 0.161.0 ± 1.42
procyanidin B24.69 ± 0.1045.1 ± 0.95
procyanidin B31.23 ± 0.0220.4 ± 0.33
procyanidin B40.827 ± 0.01815.0 ± 0.13
procyanidin B2-3-O-gallate0.0271 ± 0.01061.80 ± 0.06
procyanidin B2-3′-O-gallate0.0258 ± 0.00281.61 ± 0.01
procyanidin C11.07 ± 0.047.07 ± 0.08
procyanidin T21.24 ± 0.096.81 ± 0.06
tyrosol18.9 ± 1.3nd
p-coumaric acidb0.36 ± 0.010.71 ± 0.18
coutaric acid2.00 ± 0.12nd
caftaric acid0.192 ± 0.071nd
   
Anthocyanins  
delphinidin-3-O-glucoside0.568 ± 0.012nd
cyanidin-3-O-glucoside0.265 ± 0.010nd
petunidin-3-O-glucoside1.47 ± 0.03nd
malvidin-3-O-glucoside9.01 ± 0.50nd
malvidin-3-O-(6″-acetyl) glucoside1.92 ± 0.02nd
malvidin-3-O-(6″-p-coumaroyl) glucoside1.24 ± 0.01nd
quercetin22.4 ± 0.6nd
kaempferol0.0366 ± 0.0055nd
myricetin2.55 ± 0.07nd
quercetin-3-O-glucoside0.137 ± 0.023nd
quercetin-3-O-galactoside0.107 ± 0.006nd
resveratrol0.427 ± 0.020nd
resveratrol-3-O-glucoside9.17 ± 0.17nd
a

nd, not detected.

b

Determined in this study.

Bacterial Strains and Culture Conditions

Three bacterial strains including a microaerophilic, S. mutans (CECT 479), and two strict anaerobes, P. gingivalis (ATCC 33277) and F. nucleatum (DSMZ 15643), were selected as cariogenic and periodontal pathogens, respectively. Also, a facultative anaerobe S. dentisani 7746 (CECT 8313), previously characterized as oral probiotic, (14) was included.
S. dentisani 7746 and S. mutans were cultured in Brain Heart Infusion medium (BHI) (BD, Bergès, France) at 37 °C for 18 h and 5% CO2 atmosphere in the case of S. mutans. Anaerobic bacteria were cultured under anaerobic conditions (90% N2, 5% CO2, 5% H2) at 37 °C in Tryptic Soy Broth medium (TSB) (Scharlau, Barcelona, Spain), supplemented with hemein (5 μg/mL), vitamin K (1 μg/mL), yeast extract (5 mg/mL), and l-cysteine hydrochloride (0.5 mg/mL), according to ATCC specifications. F. nucleatum and P. gingivalis cultures were grown from fresh inoculum during 18 h and 72 h, respectively.

Cell Culture

Human gingival fibroblasts (HGF-1) (ATCC CRL-2014), used as the oral epithelial model in this study, were cultured in high glucose Dulbecco’s modified Eagle’s medium (DMEM) (Lonza, Basel, Switzerland) supplemented with 1% (v/v) penicillin/streptomycin solution (1:1) (Sigma-Aldrich, St. Louis, MO) and 10% (v/v) heat-inactivated fetal bovine serum (FBS) (Biowest, Nuaillé, France). Cells were maintained at 37 °C in 5% CO2 atmosphere and media was renewed every 3 days. Fibroblasts were subcultured once per week with a split ratio of 1:3 using 0.25% trypsin-EDTA solution (Sigma-Aldrich, St. Louis, MO).

Antimicrobial Study

Stock solutions of extracts and compounds mentioned above were prepared at 2 mg/mL final concentration in 4% dimethyl sulfoxide (DMSO) BHI or TSB media, depending on bacterial strain. Then, stock solutions were filtered (0.22 μM, Symta, Spain) and diluted to 1000, 500, 200, 100, 50, 25, 10 μg/mL final concentration. Microtitle assay (21) was carried out in a 96-wells plate, and 100 μL of each phenolic extract/compound was added to the pertinent well. Then, 100 μL of bacterial inoculum at 106 CFUs/mL final concentration was added. Negative (culture media without any inoculum/phenolic compound) and positive controls (bacteria without any treatment) as well as blanks (phenolic compounds dissolved in the culture media) were used to ensure the adequacy of the assay. A measurement (O.D.600 nm) as t = 0 absorbance was taken on a Multiskan FC plate reader (Thermo Scientific). The microplate was incubated according to each strain requirements for 24–42 h at 37 °C under aerobic, anaerobic, or 5% CO2 conditions, and absorbance was measured at selected intervals during 24 h, in order to determine the bacterial growth along time. MIC (minimum inhibitory concentration) and MBC (minimum bactericidal concentration) parameters were calculated and confirmed by microbial plate counting on BHI or modified TSB agar media. Assays were carried out in triplicate and three independent experiments were performed.

Cytotoxicity Assay

Cytotoxic effect of phenolic extracts and compounds at 50 and 10 μg/mL final concentration on HGF-1 fibroblasts viability was explored using the colorimetric 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay. Cells were seeded on 96-wells plate cells 24 h prior to the assay. Then, complete culture media was replaced by compounds/extracts dissolved in cell culture media without FBS. Plate was incubated for 30 min or 24 h, and then media was replaced by MTT reagent diluted on sterile Dulbecco’s Phosphate-Buffered saline (DPBS) solution (Lonza, Basel, Switzerland) (2 mg/mL). After 3 h incubation, MTT reagent was removed and ethanol–DMSO (1:1) mixture was added to dissolve formazan crystals. Absorbance was then measured at 570 nm on a Multiskan plate reader (Thermo Scientific). The absorbance ratio between cell culture treated with phenolics and the untreated control multiplied by 100 represents cell viability (percentage of control, %).

Bacterial Adherence Assay

F. nucleatum, P. gingivalis, and S. mutans were separately grown in their respective optimal conditions and all assays were carried out with single species bacterial cultures. Bacterial cells from an overnight culture (O.D.600 nm = 1) were harvested by centrifugation (4500 rpm, 10 min at 4 °C) and resuspended in sterile DPBS solution. Fibroblasts were seeded on 48-well plates 24 h prior to the assay at a density of 2 × 105 CFUs/mL. The cell monolayer was washed twice with DPBS to remove any FBS or antibiotic residue, and 0.5 mL of a mixture of pure specie bacterial suspension at 107 CFUs/mL final concentration plus phenolic extracts, pure compounds or DPBS solutions was added to each well of HGF-1 cells (100:1 ratio of bacteria per fibroblast, in agreement with previous works (22)). After 30 min of incubation, supernatants were removed and cells were washed twice with DPBS in order to remove unbound bacteria. Then, cells and bound bacteria were detached with 0.25% trypsin–EDTA solution, and the reaction was stopped by adding cold DPBS. Bacterial counts were carried out on BHI agar plates for S. mutans and S. dentisani after 24 h of incubation while counts for other pathogens were carried out in TSB agar plates, after 48 h (F. nucleatum) or 5 days (P. gingivalis) of incubation. S. mutans and S. dentisani presented differences in the morphology of their colonies, which makes it possible to clearly differentiate them during counting. Adhesion capacity was calculated as the number of adhered bacteria (CFUs/mL) relative to the total number of bacteria initially added (% adhesion = [adhered bacteria/total bacteria] × 100). Results are expressed as percentage of adherence inhibition (%), calculated as 100(1 – T1/T2), where T1 and T2 are the number of oral pathogens adhered in the presence and absence of phenolics, respectively. Assays were performed in triplicate, and three independent experiments were carried out.

Antiadherence Assays: Exclusion, Competition, and Displacement of S. mutans by S. dentisani

a. Adherence Exclusion

For the exclusion assay, 0.5 mL per well of the mixed solution of S. dentisani (∼107 CFUs/mL) and phenolic compounds or extracts were first added. After 15 min of incubation, nonbound bacteria were removed, 0.5 mL per well of S. mutans suspension (∼107 CFUs/mL) was added, and the mixture was incubated again for 15 min. Cells together with bound bacteria were then detached with trypsin–EDTA solution, and the number of oral bacteria adhered to gingival cells was determined on BHI agar plates, as described above. Results are expressed as percentage of adherence inhibition (%), calculated as 100(1 – T1/T2), where T1 and T2 are the number of oral pathogens adhered in the presence and absence of S. dentisani and phenolics, respectively. Assays were performed in triplicate, and three independent experiments were carried out.

b. Adherence Displacement

Ability of S. dentisani and phenolics to displace previously adhered S. mutans was assessed as described above but first adding S. mutans suspension (∼107 CFUs/mL) and later, S. dentisani suspension (∼107 CFUs/mL) plus phenolic extracts and compounds. Displacement of pathogen was expressed as percentage of adhesion (%) of oral pathogen in the presence and absence of S. dentisani and phenolics, as described above.

c. Adherence Competition

The same experimental protocol as in exclusion was employed for the assays of competitiveness between S. dentisani and S. mutans, with the difference that oral pathogen (∼107 CFUs/mL) and S. dentisani probiotic strain (107 CFUs/mL) plus phenolics were simultaneously added. Competitiveness was calculated as the percentage of adhesion (%) of S. mutans in combination with S. dentisani and phenolics relative to pathogen adhesion in the absence of S. dentisani and phenolic compounds (control).

UHPLC–DAD-ESI-TQ MS Targeted Analysis of Phenolic Metabolites

Incubations of cell monolayers with phenolic compounds (50 μg/mL) in absence (cellular metabolism) or presence of oral pathogens (bacterial and cellular metabolism) were carried out as mentioned above in three independent assays. After 30 min of incubation at controlled conditions, supernatants were collected and an aliquot was immediately frozen away (−80 °C) until further UHPLC–MS/MS analysis. Incubations only with phenolic compounds (blanks) or oral pathogens (bacterial metabolism) were also carried out.
Prior to their analysis, cellular supernatants were filtered (0.22 μM, Symta, Spain), and 200 μL of sample was mixed with 50 μL of internal standard (4-hydroxybenzoic-2,3,5,6-tetradeutered acid) (IS) prepared in acetonitrile and 0.1% formic acid at 0.25 μg/mL final concentration. A volume of 2.0 μL of sample was injected onto the chromatographic system. Analysis of each sample was performed in duplicate.
Phenolic metabolites were analyzed using an UPLC–ESI-MS/MS following a method previously published (23) with some modifications. The liquid chromatographic system was a Waters Acquity UPLC (Milford, MA) equipped with a binary pump, an autosampler thermostated at 10 °C, and a heated column compartment (40 °C). The column employed was a BEH-C18, 2.1 mm × 100 mm and 1.7 μm particle size from Waters (Milford, MA). The mobile phases were 0.1% formic acid in water (A) and 0.1% formic acid in acetonitrile (B). The gradient program was as follows: 0 min, 0.1% B; 1.5 min, 0.1% B; 11.17 min, 16.3% B; 11.5 min, 18.4% B; 14 min, 18.4% B; 14.1 min, 99.9% B; 16.6 min, 99.9% B; 16.7 min, 0.1% B; 22 min 0.1% B. Equilibrium time was set at 2.4 min, resulting in a total runtime of 22.4 min. The flow rate was set constant at 0.5 mL/min and injection volume was 2 μL.
The LC effluent was pumped to an Acquity TQD tandem quadrupole mass spectrometer equipped with a Z-spray electrospray ionization (ESI) source operated in negative polarity mode. The ESI parameters were set as follows: capillary voltage, 3 kV; source temperature, 130 °C; desolvation temperature, 400 °C; desolvation gas (N2) flow rate, 750 L/h; cone gas (N2) flow rate, 60 L/h. The ESI was operated in negative ionization mode. For quantification purposes, data were collected in the multiple reaction monitoring (MRM) mode, tracking the transition of parent and product ions specific to each compound. The MS/MS parameters (cone voltage, collision energy, and MRM transition) of the 54 phenolic compounds targeted in the present study (hydroxyl(phenyl)-propionic, hydroxy-(phenyl)-acetic, hydroxycinnamic, hydroxybenzoic, and hydroxymandelic acids and flavan-3-ols) were previously determined. (23) All metabolites were quantified using the calibration curves of their corresponding standards. Data acquisition were carried out in multiple reaction mode (MRM) using transition of parent and product specific ions for each compound as well as by using the internal calibration curves. Data processing was performed with MassLynx v4.1 software (Waters) and results are presented as final concentration (μg/L) of the sample.

Statistical Analysis

Data obtained were submitted to statistical analysis in GraphPad Software v6.0 (GraphPad). Two-way ANOVA of multiple comparisons was applied to data of the study of the inhibitory effect against pathogenic adherence, followed by posthoc Dunnet test. Data of UHPLC–MS/MS from the study of phenolic metabolism (three values from three independent assays, each value corresponding to the mean of the duplicate analysis of each sample) was analyzed by one-way ANOVA test followed by Bonferroni test. A value of p < 0.05 was fixed for the level of significance of the tests.

Results

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Antimicrobial Activity

Study of antimicrobial activity of phenolics against oral bacteria was assessed in order to select a concentration under the MIC for all compounds, for antiadherence assays (Table 2). (21) Phenolic compounds and extracts only showed antimicrobial activity at higher concentrations (above 200 μg/mL), and consequently, it was possible to use concentrations in the range normally found in wine, which is 0.3–33 mg/L for caffeic acid and 0.1–8 mg/L for p-coumaric acid. (24) Therefore, selected concentrations for the next assays were 10 and 50 μg/mL for each oenological extract and pure phenolic compound.
Table 2. Antimicrobial Activity of Phenolic Compounds and Grape Seed and Red Wine Phenolic Extracts
MIC/MBC (μg/mL)
microorganismscaffeic acidp-coumaric acidVitaflavanProvinols
S. mutans>1000/>1000>1000/>1000>1000/>1000>1000/>1000
P. gingivalis200/500500/1000500/1000500/>1000
F. nucleatum1000/>1000200/500500/1000500/1000
S. dentisani1000/>1000>1000/>1000>1000/>1000>1000/>1000

Cytotoxic Effect

With regards to a possible cytotoxic effect of compounds at selected concentrations on human fibroblasts, none of the phenolic compounds or extracts altered cell viability at 10 μg/mL nor 50 μg/mL (Figure 1) after 30 min of pretreatment but neither after 24 h incubation with compounds and extracts.

Figure 1

Figure 1. Cellular viability of HGF-1 fibroblasts in the presence of phenolic compounds and extracts (10 and 50 μg/mL) after 30 min and 24 h incubations. Results are expressed as media of three independent assays ± standard deviation.

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Antiadhesive Effects on Oral Pathogen Adherence to HGF-1 Human Fibroblasts

With respect to antiadhesive activity of phenolic compounds and extracts, a different effect was perceived depending on the strain, phenolic concentration, and compound (Figure 2). In general terms, pure phenolic compounds (caffeic and p-coumaric acids) showed a greater ability to inhibit S. mutans and F. nucleatum adherence than phenolic extracts, whereas a similar effect for both treatments was reported in the case of P. gingivalis adherence to human fibroblasts.

Figure 2

Figure 2. Adherence inhibition (%) of oral pathogens (A) S. mutans, (B) F. nucleatum, and (C) P. gingivalis) by phenolic compounds and extracts (10 and 50 μg/mL). Results are expressed as the media of three independent assays ± standard error. * indicates p < 0.05, ** indicates p < 0.01, and *** indicated p < 0.001.

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S. mutans pathogen is normally related to caries disease, and therefore the ability of this bacterium to adhere fibroblasts is limited, around 1% (data not shown). Despite this fact, caffeic acid and p-coumaric acid at 50 μg/mL concentrations were able to decrease S. mutans adherence 20% and 40%, respectively (p < 0.001). Both compounds had a similar effect at 10 μg/mL concentration, reaching an inhibition of around 20–30% (p < 0.001). However, phenolic extracts Vitaflavan and Provinols did not exert any inhibitory effect on S. mutans adherence, except for Vitaflavan (10 μg/mL) (p < 0.05), and even an increase of adherence was observed for the higher concentration (50 μg/mL) (values of adherence inhibition <0% are not represented).
Inhibition of P. gingivalis adherence was tested for all the assayed compounds, including both pure phenolics and extracts (Figure 2C). Phenolic compounds reached higher values of inhibition when added at 10 μg/mL concentration (p < 0.001), whereas grape seed and red wine phenolic extracts were able to exert a stronger effect when used at 50 μg/mL concentration (p < 0.001). Inhibitory effects of caffeic and p-coumaric acids were similar, in the range of 30–50%. Provinols, a red wine extract, showed higher inhibitory potential (∼40–50%) than grape seed extract (Vitaflavan) (∼20–40%). Finally, in the case of F. nucleatum adherence, compounds exerted a stronger inhibition of pathogen adherence (p values ranging from <0.05 to 0.01) than extracts, especially, in the case of p-coumaric acid (p < 0.01) which caused a marked inhibition, upper than 50%. Furthermore, Provinols (10 μg/mL, p < 0.01) inhibition values were again higher than those of Vitaflavan.
Previous studies highlighted the potential role of S. dentisani in oral diseases. (14) With the aim of studying a possible complementary effect between this candidate oral probiotic and red wine phenolic compounds against S. mutans adherence to human fibroblasts, assays of inhibition of bacterial adherence were performed (Figure 3). Results confirmed a complementary action of both caffeic acid and p-coumaric acid, and S. dentisani in the competence process against S. mutans adhesion (p < 0.05), improving values from 25% to 40–50% in the presence of the coincubation of S. dentisani and phenolics. In the same way, exclusion was improved when caffeic acid was used together with the probiotic strain (p < 0.05), reaching values of 30–40% from the initial 10%. However, phenolic compounds were not able to improve the high displacement values of S. mutans (close to 80%) when only S. dentisani was used.

Figure 3

Figure 3. Percentage (%) of exclusion, displacement and competition of S. mutans adherence by S. dentisani probiotic strain 7746 and polyphenols. Results are expressed as the media of three independent experiments ± standard error. Data were analyzed by two-way ANOVA and Bonferroni test. * indicates p < 0.05.

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Bacterial and Cellular Metabolism of Oenological Extracts and Phenolic Compounds

Results of bacterial and cellular metabolism from UHPLC–MS analysis (Tables 3–5) showed that the three pathogens studied (P. gingivalis, S. mutans, and F. nucleatum) were able to release different phenolic metabolites after their incubation with phenolic compounds and extracts. Additionally, evidence also indicates an existing cellular metabolism of polyphenols by fibroblasts, which in some cases resulted in a cumulative metabolism between oral bacteria and human cells.
Table 3. Phenolic Metabolite Concentration (μg/L) After Incubations in Absence or Presence of P. gingivalis and/or of HGF-1 Cellsa
 VitaflavanProvinolscaffeic acidp-coumaric acid
metaboliteblankbacteriumcellsbacterium + cellsblankbacteriumcellsbacterium + cellsblankbacteriumcellsbacterium + cellsblankbacteriumcellsbacterium + cells
Phenolic Acids
gallic acid884.18 ± 12.48533.82 ± 51.72**754.00 ± 115.46663.24 ± 142.11108.07 ± 20.3891.77 ± 8.73133.79 ± 51.0196.81 ± 15.13––––––––
protocatechuic acid60.79 ± 4.1145.25 ± 5.9837.85 ± 4.4941.72 ± 15.8720.45 ± 6.8113.53 ± 4.23**33.62 ± 4.4915.65 ± 6.34*––––––––
3,5-dihydroxybenzoic acid62.27 ± 3.7445.00 ± 5.6633.50 ± 7.78*44.67 ± 10.0229.46 ± 4.6414.67 ± 1.15**22.89 ± 10.21**14.33 ± 3.51**––––––––
4-hydroxyphenyl acetic acid33.26 ± 0.01389.28 ± 152.16*–418.62 ± 0.141.06*–399.06 ± 85.27*–522.95 ± 166.37*–359.94 ± 58.69*–366.46 ± 81.44*–412–10 ± 138.78*–425.14 ± 68.70*
3-(4-hydroxyphenyl) propionic acid––––––––––––14215.21 ± 2052.1514686.16 ± 555.2015593.41 ± 555.2014484.549 ± 3078.04
caffeic acid––––––––57839.67 ± 1132.0558879.37 ± 11895.3769838.04 ± 7391.3355997.27 ± 2718.09––––
p-coumaric acid67.18 ± 17.9433.06 ± 13.56*17.33 ± 5.37**34.21 ± 13.04*37.26 ± 10.1330.38 ± 3.8431.14 ± 1.0836.26 ± 3.10––––25074.57 ± 460.2523621.28 ± 2619.8225232.70 ± 1974.3823430.21 ± 2493.78
Flavan-3-ols
(+)-catechin3458.11 ± 84.413320 ± 237.153941.37 ± 414.313556.73 ± 771.64227.94 ± 22.11204.83 ± 49.66415.15 ± 200.52282.51 ± 42.92––––––––
(−)-epicatechin2876.67 ± 162.402266.12 ± 616.343362.81 ± 713.872949.40 ± 602.27208.72 ± 84.10191.39 ± 27.13189.48 ± 8.12189.48 ± 26.31––––––––
procyanidin B11718.29 ± 0.125.841508.65 ± 159.781823.56 ± 326.681685.749 ± 205.02363.75 ± 40.66206.57 ± 34.78*345.99 ± 86.58265.87 ± 70.82*––––––––
procyanidin B2973.33 ± 82.72758.29 ± 148.291152 ± 71.39927.90 ± 116.80119.99 ± 26.56126.25 ± 14.40187.34 ± 64.02115.05 ± 38.50–– –––– 
a

Data are expressed as mean values ± standard deviations. Data were analyzed by two-way ANOVA followed by the Bonferroni test. The * indicates values p < 0.05, ** indicates values p < 0.01, and *** indicates values p < 0.001; – means not detected.

Phenolic metabolism in the absence or presence of fibroblasts and P. gingivalis is presented in Table 3. Regarding oenological extracts, some compounds underwent thorough extensive metabolism during incubations. For instance, a significant degradation of gallic acid (p < 0.01) was found in the case of Vitaflavan after bacterial incubations, as in a similar manner that occurred in the case of proanthocyanidin B1 (p < 0.05) and Provinols, which reinforces the role of microbial catabolism of oligomeric tannins.
Regarding bacterial and cellular degradation of phenolic acids derived from the B-ring, 3,5-dihydroxybenzoic acid was metabolized reaching values close to 30% of degradation in the case of both oenological extracts, being especially significant in the case of Provinols (p < 0.01). In regard with nonflavonoids compounds, there was a bacterial degradation of protocatechuic acid, which was significant in the case of the incubation of P. gingivalis with Provinols extract (p < 0.01).
Additionally, 4-hydroxyphenyl acetic acid was detected only after incubations of all oenological extracts and phenolic compounds with P. gingivalis (ranging p values from <0.05 to 0.01), which highlights the potential of this bacteria to synthesize it, most likely from the catabolism of flavonols precursors.
Concerning phenolic metabolism in the presence of S. mutans (Table 4), a strong bacterial metabolism was observed for flavan-3-ols (+)-catechin (p < 0.01 to p < 0.001) and (−)-epicatechin (p < 0.01–0.001) after incubations with Vitaflavan. In a similar manner, levels of gallic acid strongly decreased after incubation of this pathogen with both extracts (p < 0.01–0.001) and also when cells or both, cells and bacteria, were present. Procyanidins B1 and B2 were markedly metabolized from Vitaflavan when cells and bacteria were simultaneously present (p < 0.001), whereas procyanidin B2 was increased in the presence of cells after treatment with Provinols (p < 0.05). In the same way, non-flavonoid protocatechuic acid from Provinols was significantly degraded after bacterial and cellular coincubations in the case of both extracts (p value ranging from p < 0.05 to p < 0.001). In relation to incubations of caffeic acid with S. mutans, a significant degradation of this compound was found (p < 0.01) only due to cumulative activity of S. mutans and HGF-1 cells.
Table 4. Phenolic Metabolite Concentration (μg/L) After Incubations with S. mutansa
 VitaflavanProvinolscaffeic acidp-coumaric acid
metaboliteblankbacteriumcellsbacterium + cellsblankbacteriumcellsbacterium + cellsblankbacteriumcellsbacterium + cellsblankbacteriumcellsbacterium + cells
Phenolic Acids
gallic acid884.18 ± 12.48147.75 ± 27.15***258.17 ± 41.27***258.17 ± 41.27***108.07 ± 20.3816.56 ± 2.03***25.77 ± 30.72***6.20 ± 2.71***––––––––
protocatechuic acid60.79 ± 4.1154.411 ± 18.2337.85 ± 4.49*14.24 ± 5.32**20.45 ± 6.8116.35 ± 5.32*22.89 ± 10.201.90 ± 0.50***––––––––
3-(4-hydroxyphenyl) propionic acid––––––––––––14215.21 ± 2052.1515831.65 ± 855.3715211.61 ± 547.4414067.54 ± 1211.78
caffeic acid––––––––57839.67 ± 1132.0569599.13 ± 2579.9469838.04 ± 7391.3327962.85 ± 3920.67**––––
p-coumaric acid67.18 ± 17.9415.28 ± 1.93**47.76 ± 12.406.08 ± 2.34***37.26 ± 10.13134.70 ± 45.69**40.85 ± 24.9351.08 ± 20.30––––25074.57 ± 460.2524640.18 ± 1696.6928867.96 ± 3155.5628011.55 ± 3324.63
Flavan-3-ols
(+)-catechin3458.11 ± 84.411349.29 ± 152.56**3906.32 ± 695.372700.28 ± 456.68227.94 ± 22.11307.15 ± 75.05*384.83 ± 8.04108.19 ± 47.67*––––––––
(−)-epicatechin2876.67 ± 162.401180.91 ± 109.60**3459.46 ± 572.472629.77 ± 412.49208.72 ± 84.10271.78 ± 106.24301.45 ± 60.90*91.87 ± 32.48––––––––
procyanidin B11718.29 ± 0.125.842357.70 ± 415.06*2067.05 ± 384.88662.76 ± 92.79***363.75 ± 40.66403.73 ± 46.23370.95 ± 224.51156.77 ± 52.58––––––––
procyanidin B2973.33 ± 82.721480.67 ± 267.96**1278.23 ± 60.59451.80 ± 115.02**119.99 ± 26.56187.00 ± 21.97224.80 ± 67.72*136.59 ± 14.26––––––––
a

Data are expressed as mean values ± standard deviations. Data were analyzed by two-way ANOVA followed by the Bonferroni test. * indicates values p < 0.05, ** indicates values p < 0.01, and *** indicates values p < 0.001; – means not detected.

Finally, data from phenolic metabolism in the absence or presence of fibroblasts and F. nucleatum assays were presented in Table 5. Metabolic activity of this bacterium seemed to be lower than the other two pathogens analyzed during this work. F. nucleatum was able to release gallic acid through bacterial catabolism (p < 0.001) from Vitaflavan extract. On the contrary to other pathogens, levels of p-coumaric acid from Vitaflavan significantly decreased after incubations with F. nucleatum (p < 0.05) or cells (p < 0.01). In accordance with results obtained from the other bacteria, levels of p-coumaric acid remained stable after incubations with the three pathogens, which resulted in a notable interest.
Table 5. Phenolic Metabolite Concentration (μg/L) After Incubations with F. nucleatum.a
 VitaflavanProvinolscaffeic acidp-coumaric acid
metaboliteblankbacteriumcellsbacterium + cellsblankbacteriumcellsbacterium + cellsblankbacteriumcellsbacterium + cellsblankbacteriumcellsbacterium + cells
Phenolic Acids
gallic acid884.18 ± 12.481667.51 ± 03.40***754.00 ± 115.462130.56 ± 108.77***108.07 ± 20.38135.47 ± 15.40133.79 ± 51.00214.05 ± 13.26***––––––––
3-(4-hydroxyphenyl) propionic acid––––––––––––14215.21 ± 2052.1517307 ± 3024.751482056 ± 1023.0716803.10 ± 2328.03
3,5-dihydroxybenzoic acid62.27 ± 3.7437.85 ± 16.4533.62 ± 7.4849.48 ± 13.2029.46 ± 4.6412.47 ± 1.5022.89 ± 10.2130.45 ± 11.58        
caffeic acid––––––––57839.67 ± 1132.0568001.98 ± 4992.3871072.47 ± 2413.9665881.80 ± 2760.38––––
p-coumaric acid67.18 ± 17.9438.04 ± 12.81*17.33 ± 5.37**53.40 ± 3.5237.26 ± 10.1325.00 ± 4.8031. 14 ±1.0841.12 ± 6.28––––25074.57 ± 460.2528203.84 ± 3086.0124505.26 ± 972.7428818.61 ± 4431.67
Flavan-3-ols
(+)-catechin3458.11 ± 84.413033.77 ± 418.033941.37 ± 414.312817.76 ± 440.73227.94 ± 22.11244.62 ± 67.35415.15 ± 200.52278.25 ± 92.52––––––––
(−)-epicatechin2876.67 ± 162.403313.05 ± 341.052951.31 ± 56.842629.77 ± 412.49208.72 ± 84.10139.72 ± 44.60189.48 ± 8.12262.21 ± 28.90*––––––––
procyanidin B11718.29 ± 125.841455.77 ± 17.001823.56 ± 326.681435.34 ± 232.38363.75 ± 40.66241.83 ± 105.44345.99 ± 86.58247.84 ± 69.60––––––––
procyanidin B2973.33 ± 82.721174.52 ± 129.181152.08 ± 84.691281.20 ± 171.45*119.99 ± 26.5680.77 ± 18.00187.34 ± 64.02127.85 ± 11.09––––––––
a

Data are expressed as mean values ± standard deviations. Data were analyzed by two-way ANOVA followed by the Bonferroni test. * indicates values p < 0.05, ** indicates values p < 0.01, and *** indicates values p < 0.001; – means not detected.

Discussion

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Previous studies discarded an antimicrobial effect of phenolic compounds and oenological extracts against gut microbial strains or respiratory pathogens in the range normally found in wine. (25,26) However, their effect on oral bacteria or on oral cells viability was unknown, and therefore, antimicrobial and cytotoxic effects were explored in the current work (Table 2, Figure 1). Antimicrobial activity of caffeic acid at high concentrations has been previously demonstrated. (24−26) However, concentrations used in our study (10 and 50 μg/mL) are not high enough to exert an antimicrobial effect against oral pathogens, and therefore, it makes it possible to study other mechanisms of action, such as the bacterial antiadhesive effect. For instance, caffeic acid was previously described to possess antimicrobial activity against S. mutans (2 mg/mL), (27) and an inhibition of cariogenic S. mutans and S. sobrinus growth by a propolis extract with elevated content of both caffeic and p-coumaric acids was reported. (28) In a similar manner, antimicrobial activity of caffeic acid (156.3 μg/mL) against pathogenic strains resistant to conventional antibiotics (Escherichia coli, Staphylococcus aureus, and Pseudomonas aeruginosa) was observed. (29) Recent evidence suggested that antimicrobial action of caffeic acid (and other phenolics, such as gallic acid and proanthocyanidins) against S. mutans could be based on the ability of polyphenols to generate hydroxyl radicals which would produce H2O2 and subsequent damage in bacterial DNA. (30) Antimicrobial effect of dietary polyphenols against periodontal pathogens has been explored too. Both grape seed and red wine extracts (>1000 μg/mL) reduced the counts of P. gingivalis and F. nucleatum, (31) whereas Muñoz-González and colleagues reported a bactericidal action of caffeic acid from red wine (1600 μg/mL) and grape seed extract (250 μg/mL) against F. nucleatum. (18) Polyphenols from different berries have been also described to inhibit F. nucleatum (>63 μg/mL) and S. mutans (>16 μg/mL). (32) However, high ranges employed on the studies mentioned above are far from physiological levels, and so other mechanisms of action should be explored. Finally, red wine was recently reported to display an antimicrobial action in an oral biofilm model containing Actynomyces oris, F. nucleatum, Streptococcus. oralis, S. mutans, and Veillonella dispar as well as against selected oral streptococci. (18,33)
A key step in bacterial infection is pathogenic adhesion to host cells, (34) and an antiadhesion therapy is an efficient way to prevent or treat bacterial infections. The percentage of adhesion of S. mutans control to human fibroblasts was around 1%, which is relatively low when compared to other species. Despite of this, our results showed that S. mutans adhesion to HGF-1 human fibroblasts was partially inhibited after treatment with caffeic (∼20–25%) and p-coumaric (∼35–40%) acids (Figure 2A). A similar study with phenolic acids of pu-erh and chrysanthemum tea enriched in tannins reported an inhibition of S. mutans attachment to oral cells and, in the same line, control adherence was around 1%. (22)S. mutans is a cariogenic pathogen and therefore is generally found on solid surfaces. Because of this, the most part of the studies regarding inhibition of bacterial attachment are carried out in solid surfaces that mimic human teeth. (35) However, last evidence suggested that it also inhabits soft oral tissues. (36) For instance, the antiadhesive effect of dealcoholized red wine over S. mutans in teeth was described, (37) and this fact was allocated to procyanidins, high weight tannins that could act as stearic impediment for S. mutans attachment. In cellular surfaces, this merge is mediated through specific receptors and bacterial attachment to cells should be high enough to facilitate the injection of bacterial virulent proteins into host cells. (34) No effect was perceived for the extracts and, in agreement with our results, a previous study carried out in a 5-species oral biofilm, including S. mutans, with Vitaflavan and Provinols reported that none of these extracts affected S. mutans viability. (18) Concerning F. nucleatum adherence, an inhibitory action of caffeic and p-coumaric acids and Provinols extract was observed (Figure 2B). In accordance, it is known that F. nucleatum adheres to a selected range of human cells, including fibroblasts and a recent study demonstrated an antiadhesive action of a green tea extract, epigallocatechin, and theaflavins against F. nucleatum adherence to oral epithelial cells. (38) The role of “physical bridge” described for this bacterium makes of the antiadhesive therapy a useful strategy to avoid periodontal diseases since it favors the attachment of other pathogens. As an example, F. nucleatum biofilm formation is stimulated by P. gingivalis due to the expression of signaling molecules, (39) as well as F. nucleatum protects P. gingivalis against aerobic conditions, by generating a capnophilic environment. (40) Therefore, the inhibition of F. nucleatum by phenolic compounds alone or in combination with S. dentisani is particularly relevant because this species has been shown to be a key player in biofilm architecture, and many periodontal pathogens use it as an attachment. (41) Thus, inhibition of F. nucleatum adhesion or growth has been proposed as a promising strategy to reduce plaque formation and prevent the settlement of oral pathogens. (42)
Our results showed that P. gingivalis adhesion to human fibroblasts was inhibited by all the assayed extracts and compounds (Figure 2C). In accordance with these observances, a high-molecular-weight fraction from cranberry, enriched in proanthocyanidins, prevented P. gingivalis attachment to surfaces coated with collagen, fibrinogen, and human serum, (43) whereas A-type proanthocyanidins from the same food source inhibited P. gingivalis adhesion to oral cells. (44) Furthermore, these compounds were able to prevent teeth demineralization during the cariogenic process. (45) Beneficial actions of resveratrol against periodontal diseases have been associated with its ability to neutralize P. gingivalis pathogenic factors. (46,47) In a similar manner, a green tea extract inhibited P. gingivalis attachment to buccal cells, (48) and also resveratrol (1–10 μM) blocked the expression of adhesion proteins of P. gingivalis. (46) In our study, resveratrol was present in red wine extract, which is in accordance with the higher inhibition of adherence observed after incubation with Provinols. In general terms, a dose-dependent inhibitory effect of pathogenic adherence was not perceived. One of the mechanisms that have been suggested for the antiadhesive potential of polyphenols is that they constitute a stearic impediment for bacterial attachment to cellular receptors. (49) There is a limited number of surface receptor of mammalian cells for bacterial adhesins, and therefore, a maximum inhibitory effect of polyphenols is going to be achieved at a specific certain concentration, and therefore, an increase in the phenolics concentration may not be necessarily translated into more effectiveness.
S. dentisani presented a similar resistance to the antimicrobial potential of the selected polyphenols to S. mutans pathogen, as shown in Table 2. This fact makes possible a combinatory study of the preventive action of wine polyphenols and this candidate oral probiotic. After coincubations with S. dentisani strain and phenolic compounds, a cumulative antiadhesive effect on S mutans was perceived (Figure 3). A reciprocal action between polyphenols and probiotics has been previously reported in the case of red wine phenolic extract and gut probiotic strains (e.g., Lactobacillus and Bifidobacterium (50) and also oenological-origin probiotic strains, which improved inhibitory effects of Provinols against E. coli adhesion to intestinal cells. (51) It is a two way interaction: probiotics are able to improve polyphenols bioavailability, (52) whereas gut microbiota is modulated by dietary polyphenols. (2,53) Our results showed that such reciprocal effect was marked for both compounds in the case of adherence competition, which suggests that polyphenols could improve the competition of S. dentisani candidate oral probiotic strain against S. mutans for cellular receptors. Additionally, a significant effect was observed with caffeic acid on the of S. mutans adherence exclusion but not on its adherence displacement, which was probably due to S. mutans being first attached to fibroblasts. These evidence highlight the potential of grape derived polyphenols as natural therapy to prevent caries and periodontal diseases, alone or in combination with traditional treatments. However, the effects mostly depend on particular combinations of phenolic structures, and it would be helpful to clarify the mechanisms of action involved on the prevention of oral diseases as well as determine the phenolic metabolism that take place in vivo, in order to design an effective strategy.
Dietary polyphenols go through several modifications along the digestive system before reaching systemic circulation, and recent evidence suggested that real executors of benefits implied from intake of dietary polyphenols are the metabolites rather than the parent compounds. (2) The most part of this phenolic metabolism takes place in the gut; however, these transformations start in the oral cavity, where dietary components suffer mechanical and chemical alterations. (2) As far as we are aware, only a little evidence has been focused on the study of oral metabolism of polyphenols, (18,54,55) and previous findings confirmed the ability of probiotic strains to metabolize oenological extracts releasing phenolic metabolites that enhanced bacterial growth. (50) Our results confirmed for the first time the relevance of bacterial and cellular phenolic metabolism as well as a complementary metabolic action (Tables 3–5). This metabolism included the degradation of precursors into phenolic metabolites as well as other enzymatic reactions. A relevant effect was perceived for bacterial metabolism of proanthocyanidins, catechins, and epicatechins. Microbial catabolism of monomeric galloylated flavan-3-ols start with the fast scission of the ester group from gallic acid by microbial esterases, which leads to the generation of pyrogallol and the monomers (+)-catechin and (−)-epicatechin. (17) A significant degradation of gallic acid, (+)-catechin, and (−)-epicatechin for S. mutans and of gallic acid by P. gingivalis was observed whereas F. nucleatum released gallic acid through esterase activity. Degradation of gallic acid by S. mutans and P. gingivalis could suggest a deeper transformation of these compounds into some other bioactive derivatives, which would prevent bacterial adhesion. In accordance with these observances, previous studies of the antimicrobial properties of red wine and grape seed extracts in an oral biofilm model revealed a bacterial metabolism of flavan-3-ols precursors, as determined by UHPLC–MS/MS. (18) Procyanidins B1 and B2 were strongly degraded after incubation with S. mutans and cells, especially in the case of Vitaflavan which is in agreement with the release and subsequent degradation of gallic acid.
Differences in the ability of oral pathogens to metabolize phenolics were perceived. For instance, S. mutans degraded gallic acid independently from phenolic source, whereas the action of P. gingivalis over this compound is moderate, which might suggest a stronger esterase and decarboxylase activities of S. mutans. 4-Hydroxyphenylacetic acid, originated from sequential α-oxidations from (hydroxyphenyl)propionic acids, was only detected due to P. gingivalis metabolism. p-Coumaric acid metabolism rarely varied: it remained stable in all the incubations, standing out as a direct effector of the inhibition of the bacterial adhesion. On the contrary, p-coumaric acid from Vitaflavan become partially degraded by P. gingivalis and S. mutans. This suggests that the wide variety of bacterial functionalities observed in vivo, might be due to the existence of bacterial consortiums rather than to the activity of isolate species. In this context, phenolic metabolism would occur in a sequential manner, leading to the production of a huge variety of chemical structures, depending on the microbial ecology present. (56) Other limiting factor in phenolic metabolism is their structural and stereo chemical characteristics, which determines the bioaccessibility to phenolic substrate. (17) Additionally, a bottleneck that limits these studies is the individual variability, in microbial composition and in physiological parameters, such as salivary composition. It is also important to point out the contribution of cellular metabolism, rarely explored. (57) In our study, a degradation of 3,5-dihydroxybenzoic acid from Provinols was perceived for P. gingivalis but only in the presence of cells or coincubations, which suggest a bacterial and cellular ability to transform it into some other derivatives, such as vanillic or hydroxybenzoic acids. In agreement with our evidence, Mena and coworked recently demonstrated the role of cellular phenolic metabolism of flavan-3-ols in the inhibition of bacterial adhesion to bladder epithelial cells. (58) Also, caffeic acid was degraded by S. mutans in the presence of cells, highlighting the cellular hydrolytic activity, together with a collaborative action with the pathogen. This is in agreement with the oxidation of caffeic acid catalyzed by cellular enzymes, such as peroxidases and tyrosinases. (59) With regard to nonflavonoids compounds, the most common microbial metabolites of caffeic acid are hydroxyphenyl propionic and protocatechuic acids. (18) Protocatechuic acid (3,4-dihydroxybenzoic acid) was partially degraded only in the presence of P. gingivalis. Additionally, the content of this compound was significantly increased in the presence of F. nucleatum, whereas coincubations with cells improved its degradation.
Study of bacterial phenolic metabolism is of high relevance in order to determine which compounds are the real inhibitors of bacterial adhesion and design an antiadhesive strategy. Furthermore, in a condition of disease, an overgrowth of pathogenic bacteria is triggered and phenolic metabolism in plaque will be mainly due to pathogenic activity. At this point, LC–MS techniques constitute a useful approach, as shown in previous research. Walle and colleagues (54) reported a release of aglycones from flavonoid glycosides (e.g., quercetin, genistein) by microbial β-glucosidases and also hydrolytic activity of oral cells by using HPLC. A similar study with LC–MS/MS revealed a contribution of human oral epithelial tissue, salivary, and microbial enzymatic activity in phenolic metabolism of anthocyanidins. (60) Our study, based on an in vitro model of bacterial adherence results, is very useful as an initial approach to go deeper into the mechanisms of action of red wine polyphenols against oral diseases. Further steps should be addressed toward the use of mixed biofilms models which can mimic bacteria–bacteria interactions as well as some other conditioning factors that should be added to multifactorial assays. Once molecular mechanisms of action become elucidated, in vivo studies of periodontal and cariogenic diseases are recommended, in order to evaluate the potential of polyphenols as preventive therapies in the management of cariogenic and periodontal diseases.

Author Information

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  • Corresponding Author
  • Authors
    • Adelaida Esteban-Fernández - Instituto de Investigación en Ciencias de la Alimentación (CIAL), CSIC-UAM, c/Nicolás Cabrera, 9, 28049 Madrid, Spain
    • Irene Zorraquín-Peña - Instituto de Investigación en Ciencias de la Alimentación (CIAL), CSIC-UAM, c/Nicolás Cabrera, 9, 28049 Madrid, Spain
    • Maria D. Ferrer - Department of Health and Genomics, Center for Advanced Research in Public Health, FISABIO Foundation, 46020 Valencia, Spain;  CIBER Epidemiology and Public Health, 28029 Madrid, Spain
    • Alex Mira - Department of Health and Genomics, Center for Advanced Research in Public Health, FISABIO Foundation, 46020 Valencia, Spain;  CIBER Epidemiology and Public Health, 28029 Madrid, Spain
    • Begoña Bartolomé - Instituto de Investigación en Ciencias de la Alimentación (CIAL), CSIC-UAM, c/Nicolás Cabrera, 9, 28049 Madrid, Spain
    • Dolores González de Llano - Instituto de Investigación en Ciencias de la Alimentación (CIAL), CSIC-UAM, c/Nicolás Cabrera, 9, 28049 Madrid, Spain
  • Funding

    This work was funded by the Spanish MINECO (Grant AGL2015-64522-C2-R project) and Comunidad de Madrid (Grant ALIBIRD-CM S2013/ABI-2728).

  • Notes
    The authors declare no competing financial interest.

Acknowledgments

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A.E-F and I.Z-P are recipients of fellowships from the FPI-MINECO Programme.

References

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    Primary prevention of cardiovascular disease with a mediterranean diet
    Estruch, Ramon; Ros, Emilio; Salas-Salvado, Jordi; Covas, Maria-Isabel; Corella, Dolores; Aros, Fernando; Gomez-Gracia, Enrique; Ruiz-Gutierrez, Valentina; Fiol, Miquel; Lapetra, Jose; Lamuela-Raventos, Rosa Maria; Serra-Majem, Lluis; Pinto, Xavier; Basora, Josep; Munoz, Miguel Angel; Sorli, Jose V.; Martinez, Jose Alfredo; Martinez-Gonzalez, Miguel Angel
    New England Journal of Medicine (2013), 368 (14), 1279-1290CODEN: NEJMAG; ISSN:0028-4793. (Massachusetts Medical Society)
    BACKGROUND Observational cohort studies and a secondary prevention trial have shown an inverse assocn. between adherence to the Mediterranean diet and cardiovascular risk. We conducted a randomized trial of this diet pattern for the primary prevention of cardiovascular events. METHODS In a multicenter trial in Spain, we randomly assigned participants who were at high cardiovascular risk, but with no cardiovascular disease at enrollment, to one of three diets: a Mediterranean diet supplemented with extra-virgin olive oil, a Mediterranean diet supplemented with mixed nuts, or a control diet (advice to reduce dietary fat). Participants received quarterly individual and group educational sessions and, depending on group assignment, free provision of extra-virgin olive oil, mixed nuts, or small nonfood gifts. The primary end point was the rate of major cardiovascular events (myocardial infarction, stroke, or death from cardiovascular causes). On the basis of the results of an interim anal., the trial was stopped after a median follow-up of 4.8 years. RESULTS A total of 7447 persons were enrolled (age range, 55 to 80 years); 57% were women. The two Mediterranean-diet groups had good adherence to the intervention, according to self-reported intake and biomarker analyses. A primary end-point event occurred in 288 participants. The multivariable-adjusted hazard ratios were 0.70 (95% confidence interval [CI], 0.54 to 0.92) and 0.72 (95% CI, 0.54 to 0.96) for the group assigned to a Mediterranean diet with extra-virgin olive oil (96 events) and the group assigned to a Mediterranean diet with nuts (83 events), resp., vs. the control group (109 events). No diet-related adverse effects were reported. CONCLUSIONS Among persons at high cardiovascular risk, a Mediterranean diet supplemented with extra-virgin olive oil or nuts reduced the incidence of major cardiovascular events.
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  4. 4
    Vázquez-Fresno, R.; Llorach, R.; Urpi-Sarda, M.; Khymenets, O.; Bulló, M.; Corella, D.; Fitó, M.; Martínez-González, M. A.; Estruch, R.; Andres-Lacueva, C. An NMR metabolomics approach reveals a combined-biomarkers model in a wine interventional trial with validation in free-living individuals of the PREDIMED study. Metabolomics 2015, 11 (4), 797– 806,  DOI: 10.1007/s11306-014-0735-x
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    An NMR metabolomics approach reveals a combined-biomarkers model in a wine interventional trial with validation in free-living individuals of the PREDIMED study
    Vazquez-Fresno, Rosa; Llorach, Rafael; Urpi-Sarda, Mireia; Khymenets, Olha; Bullo, Monica; Corella, Dolores; Fito, Montserrat; Martinez-Gonzalez, Miguel Angel; Estruch, Ramon; Andres-Lacueva, Cristina
    Metabolomics (2015), 11 (4), 797-806CODEN: METAHQ; ISSN:1573-3882. (Springer)
    The development of robust biomarkers of consumption would improve the classification of participants with regard to their dietary exposure. In addn., validation of them in free-living individuals remains an important challenge. The aim of this study is to assess wine intake biomarkers using an NMR metabolomic approach to measure the utility of these biomarkers in a wine interventional study (WIS, n = 56) and also to evaluate them in a free-living individuals (PREDIMED study, n = 91). Nine metabolites showed a significantly higher presence in urinary excretion in WIS after wine intake: five food metabolome metabolites (tartrate, Et glucuronide [EtG], 2,3-butanediol, mannitol, and ethanol); one related to the endogenous response to wine exposure (3-methyl-2-oxovalerate) and three unidentified compds. Receiver operating characteristic (ROC) curve for each single metabolite were evaluated and exhibited areas under the curves (AUC) between 67.4 and 86.3 % when they were evaluated individually. Then, a logistic regression model was fitted to generate a combined-biomarkers model using these metabolites. The model generated which included tartrate-EtG, showed an AUC of 90.7 % in WIS. Similarly, the AUC in the PREDIMED study was 92.4 %. Results showed that a model combining tartrate-EtG is more useful for evaluating exposure to wine than single biomarkers, both in interventional studies and epidemiol. data. To our knowledge, this is the first time that a combined-biomarker model using an NMR platform in wine biomarkers' research has been generated and reproduced in a free-living population.
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  5. 5
    Queipo-Ortuno, M. I.; Boto-Ordonez, M.; Murri, M.; Gomez-Zumaquero, J. M.; Clemente-Postigo, M.; Estruch, R.; Cardona Diaz, F.; Andres-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 (6), 1323– 34,  DOI: 10.3945/ajcn.111.027847
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    Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers
    Queipo-Ortuno, Maria Isabel; Boto-Ordonez, Maria; Murri, Mora; Gomez-Zumaquero, Juan Miguel; Clemente-Postigo, Mercedes; Estruch, Ramon; Diaz, Fernando Cardona; Andres-Lacueva, Cristina; Tinahones, Francisco J.
    American Journal of Clinical Nutrition (2012), 95 (6), 1323-1334CODEN: AJCNAC; ISSN:0002-9165. (American Society for Nutrition)
    Background: Few studies have investigated the effect of dietary polyphenols on the complex human gut microbiota, and they focused mainly on single polyphenol mols. and select bacterial populations. Objective: The objective was to evaluate the effect of a moderate intake of red wine polyphenols on select gut microbial groups implicated in host health benefits. Design: Ten healthy male volunteers underwent a randomized, crossover, controlled intervention study. After a washout period, all of the subjects received red wine, the equiv. amt. of de-alcoholized red wine, or gin for 20 d each. Total fecal DNA was submitted to polymerase chain reaction (PCR)-denaturing gradient gel electrophoresis and real-time quant. PCR to monitor and quantify changes in fecal microbiota. Several biochem. markers were measured. Results: The dominant bacterial compn. did not remain const. over the different intake periods. Compared with baseline, the daily consumption of red wine polyphenol for 4 wk significantly increased the no. of Enterococcus, Prevotella, Bacteroides, Bifidobacterium, Bacteroides uniformis, Eggerthella lenta, and Blautia coccoides-Eubacterium rectale groups (P < 0.05). In parallel, systolic and diastolic blood pressures and triglyceride, total cholesterol, HDL cholesterol, and C-reactive protein concns. decreased significantly (P < 0.05). Moreover, changes in cholesterol and C-reactive protein concns. were linked to changes in the bifidobacteria no. Conclusion: This study showed that red wine consumption can significantly modulate the growth of select gut microbiota in humans, which suggests possible prebiotic benefits assocd. with the inclusion of red wine polyphenols in the diet.
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    Moreno-Indias, I.; Sanchez-Alcoholado, L.; Perez-Martinez, P.; Andres-Lacueva, C.; Cardona, F.; Tinahones, F.; Queipo-Ortuno, M. I. Red wine polyphenols modulate fecal microbiota and reduce markers of the metabolic syndrome in obese patients. Food Funct. 2016, 7 (4), 1775– 1787,  DOI: 10.1039/C5FO00886G
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    Red wine polyphenols modulate fecal microbiota and reduce markers of the metabolic syndrome in obese patients
    Moreno-Indias Isabel; Cardona Fernando; Tinahones Francisco; Queipo-Ortuno Maria Isabel; Sanchez-Alcoholado Lidia; Perez-Martinez Pablo; Andres-Lacueva Cristina
    Food & function (2016), 7 (4), 1775-87 ISSN:.
    This study evaluated the possible prebiotic effect of a moderate intake of red wine polyphenols on the modulation of the gut microbiota composition and the improvement in the risk factors for the metabolic syndrome in obese patients. Ten metabolic syndrome patients and ten healthy subjects were included in a randomized, crossover, controlled intervention study. After a washout period, the subjects consumed red wine and de-alcoholized red wine over a 30 day period for each. The dominant bacterial composition did not differ significantly between the study groups after the two red wine intake periods. In the metabolic syndrome patients, red wine polyphenols significantly increased the number of fecal bifidobacteria and Lactobacillus (intestinal barrier protectors) and butyrate-producing bacteria (Faecalibacterium prausnitzii and Roseburia) at the expense of less desirable groups of bacteria such as LPS producers (Escherichia coli and Enterobacter cloacae). The changes in gut microbiota in these patients could be responsible for the improvement in the metabolic syndrome markers. Modulation of the gut microbiota by using red wine could be an effective strategy for managing metabolic diseases associated with obesity.
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    Barroso, E.; Munoz-Gonzalez, I.; Jimenez, E.; Bartolome, B.; Moreno-Arribas, M. V.; Pelaez, C.; Del Carmen Martinez-Cuesta, M.; Requena, T. Phylogenetic profile of gut microbiota in healthy adults after moderate intake of red wine. Mol. Nutr. Food Res. 2017, 61 (3), 1600620,  DOI: 10.1002/mnfr.201600620
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    Palmer, R. J., Jr. Composition and development of oral bacterial communities. Periodontol. 2000 2014, 64 (1), 20– 39,  DOI: 10.1111/j.1600-0757.2012.00453.x
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    Composition and development of oral bacterial communities
    Palmer Robert J Jr
    Periodontology 2000 (2014), 64 (1), 20-39 ISSN:.
    The oral bacterial microbiome encompasses approximately 700 commonly occurring phylotypes, approximately half of which can be present at any time in any individual. These bacteria are largely indigenous to the oral cavity; this limited habitat range suggests that interactions between the various phylotypes, and between the phylotypes and their environment, are crucial for their existence. Molecular cataloging has confirmed many basic observations on the composition of the oral microbiome that were formulated well before ribosomal RNA-based systematics, but the power and the scope of molecular taxonomy have resulted in the discovery of new phylotypes and, more importantly, have made possible a level of bacterial community analysis that was unachievable with classical methods. Bacterial community structure varies with location within the mouth, and changes in community structure are related to disease initiation and disease progression. Factors that influence the formation and the evolution of communities include selective adherence to epithelial or tooth surfaces, specific cell-to-cell binding as a driver of early community composition, and interorganismal interaction leading to alteration of the local environment, which represents the first step on the road to oral disease. A comprehensive understanding of how these factors interact to drive changes in the composition of the oral microbial community can lead to new strategies for the inhibition of periodontal diseases and dental caries.
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    Marsh, P. D.; Bradshaw, D. J. Dental plaque as a biofilm. J. Ind. Microbiol. 1995, 15 (3), 169– 75,  DOI: 10.1007/BF01569822
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    Dental plaque as a biofilm
    Marsh, P. D.; Bradshaw, D. J.
    Journal of Industrial Microbiology (1995), 15 (3), 169-75CODEN: JIMIE7; ISSN:0169-4146. (Macmillan Scientific & Medical Division)
    A review with 62 refs. Dental plaque is the diverse microbial community found on the tooth surface embedded in a matrix of polymers of bacterial and salivary origin. Once a tooth surface is cleaned, a conditioning film of proteins and glycoproteins is adsorbed rapidly to the tooth surface. Plaque formation involves the interaction between early bacterial colonizers and this film (the acquired enamel pellicle). To facilitate colonization of the tooth surface, some receptors on salivary mols. are only exposed to bacteria once the mol. is adsorbed to a surface. Subsequently, secondary colonizers adhere to the already attached early colonizers (co-aggregation) through specific mol. interactions. These can involve protein-protein or carbohydrate-protein (lectin) interactions, and this process contributes to detg. the pattern of bacterial succession. As the biofilm develops, gradients in biol. significant factors develop, and these permit the co-existence of species that would be incompatible with each other in a homogeneous environment. Dental plaque develops naturally, but it also assocd. with two of the most prevalent diseases affecting industrialized societies (caries and periodontal diseases). Future strategies to control dental plaque will be targeted to interfering with the formation, structure and pattern of development of this biofilm.
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    Esteban-Fernández, A.; Zorraquín-Peña, I.; González de Llano, D.; Bartolomé, B.; Moreno-Arribas, M. V. The role of wine and food polyphenols in oral health. Trends Food Sci. Technol. 2017, 69 (Part A), 118– 130,  DOI: 10.1016/j.tifs.2017.09.008
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    The role of wine and food polyphenols in oral health
    Esteban-Fernandez, Adelaida; Zorraquin-Pena, Irene; Gonzalez de Llano, Dolores; Bartolome, Begona; Moreno-Arribas, M. Victoria
    Trends in Food Science & Technology (2017), 69 (Part_A), 118-130CODEN: TFTEEH; ISSN:0924-2244. (Elsevier Ltd.)
    A review. There is a growing interest in understanding the human oral microbiome, due to its important role in promoting health, as reported in a no. of studies. Several factors can affect the compn. of the oral microbiota (e.g. hygienic habits, genetics, environment ...). Among them, diet is one of the most significant external factors that modulate oral microbiota, thereby affecting the balance between host health and disease. Although the compn. of oral microbiota can be considered dynamic, there is an equil. between commensal bacteria and pathogens on which oral health status relies. This study emphasizes the alteration of the balance previously mentioned, when the pathogenic bacteria population increases to the detriment of beneficial commensal bacteria, which prompts microbial-derived oral diseases such as caries, gingivitis and periodontitis that may affect every human at some point in life. Dietary polyphenols and, in particular, wine polyphenols seem to modulate the compn. of the oral microbiota suggesting plausible benefits in the prevention of caries and periodontal diseases. However, at this point, knowledge is still preliminary, and more research needs to be conducted at different levels. This review focuses on the current research regarding polyphenols and their role in preventing microbial-derived oral diseases. It gives a holistic view that emphasizes the interactions of these bioactive compds. among oral pathogens as well as their potential metab. by oral bacteria.
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    Takahashi, N.; Nyvad, B. The role of bacteria in the caries process: ecological perspectives. J. Dent. Res. 2011, 90 (3), 294– 303,  DOI: 10.1177/0022034510379602
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    The role of bacteria in the caries process: ecological perspectives
    Takahashi N; Nyvad B
    Journal of dental research (2011), 90 (3), 294-303 ISSN:.
    Dental biofilms produce acids from carbohydrates that result in caries. According to the extended caries ecological hypothesis, the caries process consists of 3 reversible stages. The microflora on clinically sound enamel surfaces contains mainly non-mutans streptococci and Actinomyces, in which acidification is mild and infrequent. This is compatible with equilibrium of the demineralization/remineralization balance or shifts the mineral balance toward net mineral gain (dynamic stability stage). When sugar is supplied frequently, acidification becomes moderate and frequent. This may enhance the acidogenicity and acidurance of the non-mutans bacteria adaptively. In addition, more aciduric strains, such as 'low-pH' non-mutans streptococci, may increase selectively. These microbial acid-induced adaptation and selection processes may, over time, shift the demineralization/remineralization balance toward net mineral loss, leading to initiation/progression of dental caries (acidogenic stage). Under severe and prolonged acidic conditions, more aciduric bacteria become dominant through acid-induced selection by temporary acid-impairment and acid-inhibition of growth (aciduric stage). At this stage, mutans streptococci and lactobacilli as well as aciduric strains of non-mutans streptococci, Actinomyces, bifidobacteria, and yeasts may become dominant. Many acidogenic and aciduric bacteria are involved in caries. Environmental acidification is the main determinant of the phenotypic and genotypic changes that occur in the microflora during caries.
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    Loesche, W. J. Microbiology of Dental Decay and Periodontal Disease. In Medical Microbiology, 4th ed.; Baron, S., Ed.; University of Texas Medical Branch at Galveston: Galveston, TX, 1996.
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    López-López, A.; Camelo-Castillo, A.; Ferrer, M. D.; Simon-Soro, Á.; Mira, A. Health-Associated Niche Inhabitants as Oral Probiotics: The Case of Streptococcus dentisani. Front. Microbiol. 2017, 8, 379,  DOI: 10.3389/fmicb.2017.00379
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    Health-Associated Niche Inhabitants as Oral Probiotics: The Case of Streptococcus dentisani
    Lopez-Lopez Arantxa; Camelo-Castillo Anny; Ferrer Maria D; Simon-Soro Aurea; Mira Alex
    Frontiers in microbiology (2017), 8 (), 379 ISSN:1664-302X.
    Oral diseases, including dental caries and periodontitis, are among the most prevalent diseases worldwide and develop as a consequence of a microbial dysbiosis. Several bacterial strains are being tested as potential oral health-promoting organisms, but usually they are species isolated from niches other than the site where they must exert its probiotic action, typically from fecal samples. We hypothesize that oral inhabitants associated to health conditions will be more effective than traditional, gut-associated probiotic species in key aspects such as colonization of the oral site where disease takes place or the possession of oral health promoting functions, as well as more practical issues like safety and toxicity, and establishing proper doses for administration. As an example of these active colonizers, we describe the case of Streptococcus dentisani, a new streptococcal species isolated from dental plaque of caries-free individuals. We have detected it in 98% of dental plaque samples from healthy individuals and, as expected, it does not produce any toxic secondary metabolite and does not survive a simulated stomach digestion, preventing potential secondary effects. Besides, this species has a double probiotic action, as it inhibits the growth of major oral pathogens through the production of bacteriocins, and also buffers acidic pH (the primary cause of dental caries) through an arginolytic pathway. We propose the use of S. dentisani as a promising probiotic against tooth decay.
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    Gupta, N. D.; Sharma, S.; Sharma, V. K. Probiotic – An emerging therapy in recolonizing periodontal pocket. Journal of Oral Biology and Craniofacial Research 2017, 7 (1), 72– 73,  DOI: 10.1016/j.jobcr.2016.09.002
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    Probiotic - An emerging therapy in recolonizing periodontal pocket
    Gupta N D; Sharma Shweta; Sharma Vivek Kumar
    Journal of oral biology and craniofacial research (2017), 7 (1), 72-73 ISSN:2212-4268.
    One of the etiological factors in the pathogenesis of periodontitis is reduction or the absence of the so-called "beneficial bacteria". Most of the globally applied treatment approach is based on subgingival bacterial elimination but recolonization with less pathogenic bacteria is seen within weeks. Therefore, researchers have started focusing on shifting the current treatment approach from specific bacterial elimination to restoring periodontal pocket with beneficial bacteria. This alteration in the ecology of niches from the one with the pathological plaque to the one with the biofilm of commensals can be achieved via subgingival application of probiotics. This article suggests the important prospects of subgingival delivery of probiotics in guiding periodontal recolonization with beneficial bacteria and emphasizes research in this study field.
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    Burton, J. P.; Wescombe, P. A.; Moore, C. J.; Chilcott, C. N.; Tagg, J. R. Safety Assessment of the Oral Cavity Probiotic Streptococcus salivarius K12. Appl. Environ. Microbiol. 2006, 72 (4), 3050– 3053,  DOI: 10.1128/AEM.72.4.3050-3053.2006
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    Monagas, M.; Urpi-Sarda, M.; Sanchez-Patan, F.; Llorach, R.; Garrido, I.; Gomez-Cordoves, C.; Andres-Lacueva, C.; Bartolome, B. Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites. Food Funct. 2010, 1 (3), 233– 53,  DOI: 10.1039/c0fo00132e
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    17
    Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites
    Monagas, Maria; Urpi-Sarda, Mireia; Sanchez-Patan, Fernando; Llorach, Rafael; Garrido, Ignacio; Gomez-Cordoves, Carmen; Andres-Lacueva, Cristina; Bartolome, Begona
    Food & Function (2010), 1 (3), 233-253CODEN: FFOUAI; ISSN:2042-6496. (Royal Society of Chemistry)
    A review. Flavan-3-ols, occurring in monomeric, as well as in oligomeric and polymeric forms (also known as condensed tannins or proanthocyanidins), are among the most abundant and bioactive dietary polyphenols, but their in vivo health effects in humans may be limited because of their recognition as xenobiotics. Bioavailability of flavan-3-ols is largely influenced by their d.p.; while monomers are readily absorbed in the small intestine, oligomers and polymers need to be biotransformed by the colonic microbiota before absorption. Therefore, phenolic metabolites, rather than the original high mol. wt. compds. found in foods, may be responsible for the health effects derived from flavan-3-ol consumption. Flavan-3-ol phenolic metabolites differ in structure, amt. and excretion site. Phase II or tissular metabolites derived from the small intestine and hepatic metab. are presented as conjugated derivs. (glucuronic acid or sulfate esters, Me ether, or their combined forms) of monomeric flavan-3-ols and are preferentially eliminated in the bile, whereas microbial metabolites are rather simple conjugated lactones and phenolic acids that are largely excreted in urine. Although the colon is seen as an important organ for the metab. of flavan-3-ols, the microbial catabolic pathways of these compds. are still under consideration, partly due to the lack of identification of bacteria with such capacity. Studies performed with synthesized or isolated phase II conjugated metabolites have revealed that they could have an effect beyond their antioxidant properties, by interacting with signalling pathways implicated in important processes involved in the development of diseases, among other bioactivities. However, the biol. properties of microbe-derived metabolites in their actual conjugated forms remain largely unknown. Currently, there is an increasing interest in their effects on intestinal infections, inflammatory intestinal diseases and overall gut health. The present review will give an insight into the metab. and microbial biotransformation of flavan-3-ols, including tentative catabolic pathways and aspects related to the identification of bacteria with the ability to catabolize these kinds of polyphenols. Also, the in vitro bioactivities of phase II and microbial phenolic metabolites will be covered in detail.
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    Muñoz-González, I.; Thurnheer, T.; Bartolomé, B.; Moreno-Arribas, M. V. Red Wine and Oenological Extracts Display Antimicrobial Effects in an Oral Bacteria Biofilm Model. J. Agric. Food Chem. 2014, 62 (20), 4731– 4737,  DOI: 10.1021/jf501768p
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    Sánchez-Patán, F.; Cueva, C.; Monagas, M.; Walton, G. E.; Gibson M, G. R.; Quintanilla-López, J. E.; Lebrón-Aguilar, R.; Martín-Álvarez, P. J.; Moreno-Arribas, M. V.; Bartolomé, B. In Vitro Fermentation of a Red Wine Extract by Human Gut Microbiota: Changes in Microbial Groups and Formation of Phenolic Metabolites. J. Agric. Food Chem. 2012, 60 (9), 2136– 2147,  DOI: 10.1021/jf2040115
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    In vitro fermentation of a red wine extract by human gut microbiota: Changes in microbial groups and formation of phenolic metabolites
    Sanchez-Patan, Fernando; Cueva, Carolina; Monagas, Maria; Walton, Gemma E.; Gibson M., Glenn R.; Quintanilla-Lopez, Jesus E.; Lebron-Aguilar, Rosa; Martin-Alvarez, P. J.; Moreno-Arribas, M. Victoria; Bartolome, Begona
    Journal of Agricultural and Food Chemistry (2012), 60 (9), 2136-2147CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
    An in vitro batch culture fermn. expt. was conducted with fecal inocula from three healthy volunteers in the presence and absence of a red wine ext. Changes in main bacterial groups were detd. by FISH during a 48 h fermn. period. The catabolism of main flavonoids (i.e., flavan-3-ols and anthocyanins) and the formation of a wide a range of phenolic microbial metabolites were detd. by a targeted UPLC-PAD-ESI-TQ MS method. Statistical anal. revealed that catechol/pyrocatechol, as well as 4-hydroxy-5-(phenyl)-valeric, 3- and 4-hydroxyphenylacetic, phenylacetic, phenylpropionic, and benzoic acids, showed the greatest increases in concn. during fermn., whereas 5-(3'-hydroxyphenyl)-γ-valerolactone, its open form 4-hydroxy-5-(3'-hydroxyphenyl)-valeric acid, and 3,4-dihydroxyphenylacetic acid represented the largest interindividual variations in the catabolism of red wine polyphenols. Despite these changes, microbial catabolism did not produce significant changes in the main bacterial groups detected, although a slight inhibition of the Clostridium histolyticum group was obsd.
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  20. 20
    Sánchez-Patán, F.; Cueva, C.; Monagas, M.; Walton, G. E.; Gibson, G. R.; Martín-Álvarez, P. J.; Victoria Moreno-Arribas, M.; Bartolomé, B. Gut microbial catabolism of grape seed flavan-3-ols by human faecal microbiota. Targetted analysis of precursor compounds, intermediate metabolites and end-products. Food Chem. 2012, 131 (1), 337– 347,  DOI: 10.1016/j.foodchem.2011.08.011
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    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 (2–3), 426– 431,  DOI: 10.1016/j.ijfoodmicro.2011.01.016
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    Comparative study of the inhibitory effects of wine polyphenols on the growth of enological lactic acid bacteria
    Garcia-Ruiz, Almudena; Moreno-Arribas, M. Victoria; Martin-Alvarez, Pedro J.; Bartolome, Begona
    International Journal of Food Microbiology (2011), 145 (2-3), 426-431CODEN: IJFMDD; ISSN:0168-1605. (Elsevier B.V.)
    This paper reports a comparative study of the inhibitory potential of 18 phenolic compds., including hydroxybenzoic acids and their derivs., hydroxycinnamic acids, phenolic alcs. and other related compds., stilbenes, flavan-3-ols and flavonols, on different lactic acid bacteria (LAB) strains of the species Oenococcus oeni, Lactobacillus hilgardii and Pediococcus pentosaceus isolated from wine. In general, flavonols and stilbenes showed the greatest inhibitory effects (lowest IC50 values) on the growth of the strains tested (0.160-0.854 for flavonols and 0.307-0.855 g/L for stilbenes). Hydroxycinnamic acids (IC50 > 0.470 g/L) and hydroxybenzoic acids and esters (IC50 > 1 g/L) exhibited medium inhibitory effect, and phenolic alcs. (IC50 > 2 g/L) and flavanol-3-ols (negligible effect) showed the lowest effect on the growth of the LAB strains studied. In comparison to the antimicrobial additives used in winemaking, IC50 values of most phenolic compds. were higher than those of potassium metabisulphite for O. oeni strains (e.g., around 4-fold higher for quercetin than for potassium metabisulphite), but lower for L. hilgardii and P. pentosaceus strains (e.g., around 2-fold lower for quercetin). Lysozyme IC50 values were negligible for L. hilgardii and P. pentosaceus, and were higher than those corresponding to most of the phenolic compds. tested for O. oeni strains, indicating that lysozyme was less toxic for LAB than the phenolic compds. in wine. SEM confirmed damage of the cell membrane integrity as a consequence of the incubation with antimicrobial agents. These results contribute to the understanding of the inhibitory action of wine phenolics on the progress of malolactic fermn., and also to the development of new alternatives to the use of sulfites in enol.
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  22. 22
    Wang, Y.; Chung, F. F.; Lee, S. M.; Dykes, G. A. Inhibition of attachment of oral bacteria to immortalized human gingival fibroblasts (HGF-1) by tea extracts and tea components. BMC Res. Notes 2013, 6, 143,  DOI: 10.1186/1756-0500-6-143
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    22
    Inhibition of attachment of oral bacteria to immortalized human gingival fibroblasts (HGF-1) by tea extracts and tea components
    Wang Yi; Chung Felicia F L; Lee Sui M; Dykes Gary A
    BMC research notes (2013), 6 (), 143 ISSN:.
    BACKGROUND: Tea has been suggested to promote oral health by inhibiting bacterial attachment to the oral cavity. Most studies have focused on prevention of bacterial attachment to hard surfaces such as enamel. FINDINGS: This study investigated the effect of five commercial tea (green, oolong, black, pu-erh and chrysanthemum) extracts and tea components (epigallocatechin gallate and gallic acid) on the attachment of five oral pathogens (Streptococcus mutans ATCC 25175, Streptococcus mutans ATCC 35668, Streptococcus mitis ATCC 49456, Streptococcus salivarius ATCC 13419 and Actinomyces naeslundii ATCC 51655) to the HGF-1 gingival cell line. Extracts of two of the teas (pu-erh and chrysanthemum) significantly (p < 0.05) reduced attachment of all the Streptococcus strains by up to 4 log CFU/well but effects of other teas and components were small. CONCLUSIONS: Pu-erh and chrysanthemum tea may have the potential to reduce attachment of oral pathogens to gingival tissue and improve the health of oral soft tissues.
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    Muñoz-González, I.; Jiménez-Girón, A.; Martín-Álvarez, P. J.; Bartolomé, B.; Moreno-Arribas, M. V. Profiling of Microbial-Derived Phenolic Metabolites in Human Feces after Moderate Red Wine Intake. J. Agric. Food Chem. 2013, 61 (39), 9470– 9479,  DOI: 10.1021/jf4025135
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    García-Ruiz, A.; Bartolomé, B.; Martínez-Rodríguez, A. J.; Pueyo, E.; Martín-Álvarez, P. J.; Moreno-Arribas, M. V. Potential of phenolic compounds for controlling lactic acid bacteria growth in wine. Food Control 2008, 19 (9), 835– 841,  DOI: 10.1016/j.foodcont.2007.08.018
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    Cueva, C.; Moreno-Arribas, M. V.; Martin-Alvarez, P. J.; Bills, G.; Vicente, M. F.; Basilio, A.; Rivas, C. L.; Requena, T.; Rodriguez, J. M.; Bartolome, B. Antimicrobial activity of phenolic acids against commensal, probiotic and pathogenic bacteria. Res. Microbiol. 2010, 161 (5), 372– 82,  DOI: 10.1016/j.resmic.2010.04.006
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    Antimicrobial activity of phenolic acids against commensal, probiotic and pathogenic bacteria
    Cueva, Carolina; Moreno-Arribas, M. Victoria; Martin-Alvarez, Pedro J.; Bills, Gerald; Vicente, M. Francisca; Basilio, Angela; Rivas, Concepcion Lopez; Requena, Teresa; Rodriguez, Juan M.; Bartolome, Begona
    Research in Microbiology (2010), 161 (5), 372-382CODEN: RMCREW; ISSN:0923-2508. (Elsevier Masson SAS)
    Phenolic acids (benzoic, phenylacetic and phenylpropionic acids) are the most abundant phenolic structures found in fecal water. As an approach towards the exploration of their action in the gut, this paper reports the antimicrobial activity of thirteen phenolic acids towards Escherichia coli, Lactobacillus spp., Staphylococcus aureus, Pseudomonas aeruginosa and Candida albicans. The growth of E. coli ATCC 25922 was inhibited by only four of the phenolic acids tested at a concn. of 1000 μg/mL, whereas pathogenic E. coli O157:H7 (CECT 5947) was susceptible to ten of them. The genetically manipulated E. coli lpxC/tolC strain was highly susceptible to phenolic acids. The growth of lactobacilli (Lactobacillus paraplantarum LCH7, Lactobacillus plantarum LCH17, Lactobacillus fermentum LPH1, L. fermentum CECT 5716, Lactobacillus brevis LCH23, and Lactobacillus coryniformis CECT 5711) and pathogens (S. aureus EP167 and C. albicans MY1055) was also inhibited by phenolic acids, but to varying extents. Only P. aeruginosa PAO1 was not susceptible to any of the phenolic compds. tested. Structure-activity relationships of phenolic acids and some of their diet precursors [(+)-catechin and (-)-epicatechin] were established, based on multivariate anal. of microbial activities. The antimicrobial properties of phenolic acids reported in this paper might be relevant in vivo.
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    Cueva, C.; Mingo, S.; Munoz-Gonzalez, I.; Bustos, I.; Requena, T.; del Campo, R.; Martin-Alvarez, P. J.; Bartolome, B.; Moreno-Arribas, M. V. Antibacterial activity of wine phenolic compounds and oenological extracts against potential respiratory pathogens. Lett. Appl. Microbiol. 2012, 54 (6), 557– 63,  DOI: 10.1111/j.1472-765X.2012.03248.x
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    26
    Antibacterial activity of wine phenolic compounds and oenological extracts against potential respiratory pathogens
    Cueva, C.; Mingo, S.; Munoz-Gonzalez, I.; Bustos, I.; Requena, T.; del Campo, R.; Martin-Alvarez, P. J.; Bartolome, B.; Moreno-Arribas, M. V.
    Letters in Applied Microbiology (2012), 54 (6), 557-563CODEN: LAMIE7; ISSN:0266-8254. (Wiley-Blackwell)
    The aim was to investigate the effect of seven wine phenolic compds. and six oenol. phenolic exts. on the growth of pathogenic bacteria assocd. with respiratory diseases (Pseudomonas aeruginosa, Staphylococcus aureus, Moraxella catarrhalis, Enterococcus faecalis, Streptococcus sp Group F, Streptococcus agalactiae and Streptococcus pneumoniae). Antimicrobial activity was detd. using a microdilution method and quantified as IC50. Mor. catarrhalis was the most susceptible specie to phenolic compds. and exts. Gallic acid and Et gallate were the compds. that showed the greatest antimicrobial activity. Regarding phenolic exts., GSE (grape seed ext.) and GSE-O (oligomeric-rich fraction from GSE) were the ones that displayed the strongest antimicrobial effects. Results highlight the antimicrobial properties of wine phenolic compds. and oenol. exts. against potential respiratory pathogens. The antimicrobial activity of wine phenolic compds. was influenced by the type of phenolic compds. Gram-neg. bacteria were more susceptible than Gram-pos. bacteria to the action of phenolic compds. and exts.; however, the effect was species-dependent. The ability to inhibit the growth of respiratory pathogenic bacteria as shown by several wine phenolic compds. and oenol. exts. warrants further investigations to explore the use of grape and wine prepns. in oral hygiene.
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    Almeida, A. A. P.; Naghetini, C. C.; Santos, V. R.; Antonio, A. G.; Farah, A.; Glória, M. B. A. Influence of natural coffee compounds, coffee extracts and increased levels of caffeine on the inhibition of Streptococcus mutans. Food Res. Int. 2012, 49 (1), 459– 461,  DOI: 10.1016/j.foodres.2012.07.026
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    Influence of natural coffee compounds, coffee extracts and increased levels of caffeine on the inhibition of Streptococcus mutans
    Almeida, A. A. P.; Naghetini, C. C.; Santos, V. R.; Antonio, A. G.; Farah, A.; Gloria, M. B. A.
    Food Research International (2012), 49 (1), 459-461CODEN: FORIEU; ISSN:0963-9969. (Elsevier B.V.)
    The inhibition of Streptococcus mutans by Coffea arabica exts. incorporated or not with natural coffee compds. was investigated by the disk diffusion method. Addnl., the turbidimetric test was used to verify the influence of caffeine concn. on the inhibition of S. mutans. Exts. of different samples of Arabica coffee showed antibacterial activity against S. mutans. The inhibitory effect was not affected by the brewing method (filtered or espresso) or by the different Arabica coffee samples. Plain caffeine, trigonelline, caffeic acid, protocatechuic acid and chlorogenic acid at 2.0 mg/mL provided similar antimicrobial effect against S. mutans. However, there was an increase in the antibacterial activity when these compds. were added to the coffee ext., except for chlorogenic acid which did not affect the inhibitory effect. Caffeine at concns. found in Arabica beverages inhibited S. mutans temporarily, whereas higher caffeine concns. provided a stronger and longer lasting inhibition.
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    Barrientos, L.; Herrera, C. L.; Montenegro, G.; Ortega, X.; Veloz, J.; Alvear, M.; Cuevas, A.; Saavedra, N.; Salazar, L. A. Chemical and botanical characterization of Chilean propolis and biological activity on cariogenic bacteria Streptococcus mutans and Streptococcus sobrinus. Braz. J. Microbiol. 2013, 44 (2), 577– 85,  DOI: 10.1590/S1517-83822013000200038
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    Chemical and botanical characterization of Chilean propolis and biological activity on cariogenic bacteria Streptococcus mutans and Streptococcus sobrinus
    Barrientos, Leticia; Herrera, Christian L.; Montenegro, Gloria; Ortega, Ximena; Veloz, Jorge; Alvear, Marysol; Cuevas, Alejandro; Saavedra, Nicolas; Salazar, Luis A.
    Brazilian Journal of Microbiology (2013), 44 (2), 577-585, 9 pp.CODEN: BJMRAH; ISSN:1517-8382. (Brazilian Society of Microbiology)
    Propolis is a non-toxic natural substance with multiple pharmacol. properties including anticancer, antioxidant, fungicidal, antibacterial, antiviral and anti-inflammatory among others. The aim of this study was to det. the chem. and botanical characterization of Chilean propolis samples and to evaluate their biol. activity against the cariogenic bacteria Streptococcus mutans and Streptococcus sobrinus. Twenty propolis samples were obtained from beekeeping producers from the central and southern regions of Chile. The botanical profile was detd. by palynol. anal. Total phenolic contents were detd. using colorimetric assays. Reverse phase HPLC and HPLC-MS were used to det. the chem. compn. The min. inhibitory concn. (MIC) was detd. on S. mutans and S. sobrinus. All propolis samples were dominated by structures from native plant species. The characterization by HPLC/MS, evidenced the presence of quercetin, myricetin, kaempferol, rutine, pinocembrin, coumaric acid, caffeic acid and caffeic acid phenethyl ester, that have already been described in these propolis with conventional HPLC. Although all propolis samples inhibited the mutans streptococci growth, it was obsd. a wide spectrum of action (MIC 0.90 to 8.22 μg mL-1). Given that results it becomes increasingly evident the need of standardization procedures, where we combine both the detn. of botanical and the chem. characterization of the exts. Research conducted to date, describes a promising effectiveness of propolis in the prevention of caries and other diseases of the oral cavity, making it necessary to develop studies to identify and understand the therapeutic targets or mechanisms of mol. action of the various compds. present on them.
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  29. 29
    Lima, V. N.; Oliveira-Tintino, C. D. M.; Santos, E. S.; Morais, L. P.; Tintino, S. R.; Freitas, T. S.; Geraldo, Y. S.; Pereira, R. L. S.; Cruz, R. P.; Menezes, I. R. A.; Coutinho, H. D. M. Antimicrobial and enhancement of the antibiotic activity by phenolic compounds: Gallic acid, caffeic acid and pyrogallol. Microb. Pathog. 2016, 99, 56– 61,  DOI: 10.1016/j.micpath.2016.08.004
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    Antimicrobial and enhancement of the antibiotic activity by phenolic compounds: Gallic acid, caffeic acid and pyrogallol
    Lima, Valeria N.; Oliveira-Tintino, Cicera D. M.; Santos, Enaide S.; Morais, Luis P.; Tintino, Saulo R.; Freitas, Thiago S.; Geraldo, Yuri S.; Pereira, Raimundo L. S.; Cruz, Rafael P.; Menezes, Irwin R. A.; Coutinho, Henrique D. M.
    Microbial Pathogenesis (2016), 99 (), 56-61CODEN: MIPAEV; ISSN:0882-4010. (Elsevier Ltd.)
    The indiscriminate use of antimicrobial drugs has increased the spectrum of exposure of these organisms. In our studies, these phenolic compds. were evaluated: gallic acid, caffeic acid and pyrogallol. The antibacterial, antifungal and modulatory of antibiotic activities of these compds. were assayed using microdilution method of Min. Inhibitory Concn. (MIC) to bacteria and Min. Fungicide Concn. (MFC) to fungi. The modulation was made by comparisons of the MIC and MFC of the compds. alone and combined with drugs against bacteria and fungi resp., using a sub-inhibitory concn. of 128 μg/mL of substances (MIC/8). All substances not demonstrated clin. relevant antibacterial activity with a MIC above ≥1024 μg/mL. As a result, we obsd. that the caffeic acid presented a potentiating antibacterial effect over the 3 groups of bacteria studied. Pyrogallol showed a synergistic effect with two of the antibiotics tested, but only against Staphylococcus aureus. In general, caffeic acid was the substance that presented with the greatest no. of antibiotics and with the greatest no. of bacteria. In relation to the antifungal activity of all the compds., the verified results were ≥1024 μg/mL, not demonstrating significant activity. Regarding potentiation of the effect of fluconazole, was obsd. synergistic effect only when assayed against Candida tropicalis, with all substances. Therefore, as can be seen, the compds. presented as substances that can be promising potentiating agents of antimicrobial drugs, even though they do not have direct antibacterial and antifungal action.
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    Nakamura, K.; Ishiyama, K.; Sheng, H.; Ikai, H.; Kanno, T.; Niwano, Y. Bactericidal Activity and Mechanism of Photoirradiated Polyphenols against Gram-Positive and -Negative Bacteria. J. Agric. Food Chem. 2015, 63 (35), 7707– 13,  DOI: 10.1021/jf5058588
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    Bactericidal activity and mechanism of photoirradiated polyphenols against Gram-positive and -negative bacteria
    Nakamura, Keisuke; Ishiyama, Kirika; Sheng, Hong; Ikai, Hiroyo; Kanno, Taro; Niwano, Yoshimi
    Journal of Agricultural and Food Chemistry (2015), 63 (35), 7707-7713CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
    The bactericidal effect of various types of photoirradiated polyphenols against Gram-pos. and -neg. bacteria was evaluated in relation to the mode of action. Gram-pos. bacteria (Enterococcus faecalis, Staphylococcus aureus, and Streptococcus mutans) and Gram-neg. bacteria (Aggregatibacter actinomycetemcomitans, Escherichia coli, and Pseudomonas aeruginosa) suspended in a 1 mg/mL polyphenol aq. soln. (caffeic acid, gallic acid, chlorogenic acid, epigallocatechin, epigallocatechin gallate, and proanthocyanidin) were exposed to LED light (wavelength, 400 nm; irradiance, 260 mW/cm2) for 5 or 10 min. Caffeic acid and chlorogenic acid exerted the highest bactericidal activity followed by gallic acid and proanthocyanidin against both Gram-pos. and -neg. bacteria. It was also demonstrated that the disinfection treatment induced oxidative damage of bacterial DNA, which suggests that polyphenols are incorporated into bacterial cells. The present study suggests that blue light irradn. of polyphenols could be a novel disinfection treatment.
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    Furiga, A.; Lonvaud-Funel, A.; Badet, C. In vitro study of antioxidant capacity and antibacterial activity on oral anaerobes of a grape seed extract. Food Chem. 2009, 113 (4), 1037– 1040,  DOI: 10.1016/j.foodchem.2008.08.059
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    Ben Lagha, A.; Dudonne, S.; Desjardins, Y.; Grenier, D. Wild Blueberry (Vaccinium angustifolium Ait.) Polyphenols Target Fusobacterium nucleatum and the Host Inflammatory Response: Potential Innovative Molecules for Treating Periodontal Diseases. J. Agric. Food Chem. 2015, 63 (31), 6999– 7008,  DOI: 10.1021/acs.jafc.5b01525
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    Daglia, M.; Papetti, A.; Grisoli, P.; Aceti, C.; Dacarro, C.; Gazzani, G. Antibacterial Activity of Red and White Wine against Oral Streptococci. J. Agric. Food Chem. 2007, 55 (13), 5038– 5042,  DOI: 10.1021/jf070352q
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    Krachler, A. M.; Orth, K. Targeting the bacteria–host interface: Strategies in anti-adhesion therapy. Virulence 2013, 4 (4), 284– 294,  DOI: 10.4161/viru.24606
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    Yamanaka, A.; Kimizuka, R.; Kato, T.; Okuda, K. Inhibitory effects of cranberry juice on attachment of oral streptococci and biofilm formation. Oral Microbiol. Immunol. 2004, 19 (3), 150– 4,  DOI: 10.1111/j.0902-0055.2004.00130.x
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    Inhibitory effects of cranberry juice on attachment of oral streptococci and biofilm formation
    Yamanaka A; Kimizuka R; Kato T; Okuda K
    Oral microbiology and immunology (2004), 19 (3), 150-4 ISSN:0902-0055.
    Cranberry juice is known to inhibit bacterial adhesion. We examined the inhibitory effect of cranberry juice on the adhesion of oral streptococci strains labeled with [3H]-thymidine to saliva-coated hydroxyapatite beads (s-HA). When the bacterial cells were momentarily exposed to cranberry juice, their adherence to s-HA decreased significantly compared with the control (P < 0.01). Their hydrophobicity also decreased dependently with the concentration of cranberry juice. We also evaluated the inhibitory effect of cranberry juice on biofilm formation. By using a microplate system, we found that the high molecular mass constituents of cranberry juice inhibited the biofilm formation of the tested streptococci. The inhibitory activity was related to the reduction of the hydrophobicity. The present findings suggest that cranberry juice component(s) can inhibit colonization by oral streptococci to the tooth surface and can thus slow development of dental plaque.
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    Berlutti, F.; Catizone, A.; Ricci, G.; Frioni, A.; Natalizi, T.; Valenti, P.; Polimeni, A. Streptococcus mutans and Streptococcus sobrinus are able to adhere and invade human gingival fibroblast cell line. Int. J. Immunopathol. Pharmacol. 2010, 23 (4), 1253– 60,  DOI: 10.1177/039463201002300430
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    Streptococcus mutans and Streptococcus sobrinus are able to adhere and invade human gingival fibroblast cell line
    Berlutti F; Catizone A; Ricci G; Frioni A; Natalizi T; Valenti P; Polimeni A
    International journal of immunopathology and pharmacology (2010), 23 (4), 1253-60 ISSN:0394-6320.
    Streptococcus mutans and Streptococcus sobrinus, the principal etiologic agents of caries decay of teeth, are generally acquired in oral cavity at the moment of tooth eruption. However, as S. mutans has been detected in oral cavity of predentate children, the eruption of teeth seems not to be a necessary prerequisite, suggesting that this species may be not confined to dental plaque. Here, we evaluate the ability of S. mutans and S. sobrinus in planktonic and biofilm lifestyle to adhere, invade and survive within human gingival fibroblast (HGF-1) cells. Planktonic and biofilm streptococci adhered and invaded host cells to different extents, showing higher efficiencies of biofilm than planktonic counterparts. Moreover, planktonic and biofilm streptococci showed the same percentage of survival within host cells. Transmission electron and confocal microscopy observations confirmed intracellular localization of planktonic and biofilm bacteria. The adhesion, invasion and survival abilities within human oral cells may be considered S. mutans and S. sobrinus virulence mechanisms to colonize and persist in the oral cavity in the absence of tooth surface.
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    Daglia, M.; Stauder, M.; Papetti, A.; Signoretto, C.; Giusto, G.; Canepari, P.; Pruzzo, C.; Gazzani, G. Isolation of red wine components with anti-adhesion and anti-biofilm activity against Streptococcus mutans. Food Chem. 2010, 119 (3), 1182– 1188,  DOI: 10.1016/j.foodchem.2009.08.037
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    Ben Lagha, A.; Haas, B.; Grenier, D. Sci. Rep. 2017, 7, 44815,  DOI: 10.1038/srep44815
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    Tea polyphenols inhibit the growth and virulence properties of Fusobacterium nucleatum
    Ben Lagha, Amel; Haas, Bruno; Grenier, Daniel
    Scientific Reports (2017), 7 (), 44815CODEN: SRCEC3; ISSN:2045-2322. (Nature Publishing Group)
    Fusobacterium nucleatum plays a key role in creating the pathogenic subgingival biofilm that initiates destructive periodontitis. It is also a common resident of the human gastrointestinal tract and has been assocd. with inflammatory bowel disease. The aim of the present study was to investigate the effects of green and black tea exts. as well as two of their bioactive components, EGCG and theaflavins, on the growth and virulence properties of F. nucleatum. The tea exts. and components displayed various degrees of antibacterial activity that may involve damage to the bacterial cell membrane and the chelation of iron. They also prevented biofilm formation by F. nucleatum at concns. that did not interfere with bacterial growth. In addn., the treatment of a pre-formed F. nucleatum biofilm with the green tea ext. and EGCG caused a time-dependent decrease in biofilm viability. The green and black tea exts., EGCG, and theaflavins decreased the adherence of F. nucleatum to oral epithelial cells and matrix proteins. Moreover, these tea components also attenuated F. nucleatum-mediated hemolysis and hydrogen sulfide prodn., two other virulence factors expressed by this bacterium. In summary, this study showed that tea polyphenols may be of interest for treating F. nucleatum-assocd. disorders.
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    Saito, Y.; Fujii, R.; Nakagawa, K. I.; Kuramitsu, H. K.; Okuda, K.; Ishihara, K. Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis. Oral Microbiol. Immunol. 2008, 23 (1), 1– 6,  DOI: 10.1111/j.1399-302X.2007.00380.x
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    Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis
    Saito Y; Fujii R; Nakagawa K-I; Kuramitsu H K; Okuda K; Ishihara K
    Oral microbiology and immunology (2008), 23 (1), 1-6 ISSN:0902-0055.
    BACKGROUND/AIMS: Bacterial infection is a major cause of periapical periodontitis. Eradication of these microorganisms from apical lesions is essential to the success of endodontic treatment. The aim of this study was to clarify the molecular interaction between Fusobacterium nucleatum, Porphyromonas gingivalis and other microorganisms associated with periapical periodontitis. METHODS: Microorganisms isolated from periapical lesions were inoculated into type-I collagen-coated polystyrene microtiter plates and maintained at 37 degrees C under anaerobic conditions for 2 days, after which, the quantity of organized biofilm on the plates was evaluated by crystal violet staining. Growth enhancement via soluble factor was evaluated by separated coculture using a 0.4-mum membrane filter. RESULTS: F. nucleatum exhibited strong adherence to type-I collagen-coated polystyrene microplates. Biofilm formation by F. nucleatum was significantly enhanced by P. gingivalis. It was complemented by compartmentalized coculture with P. gingivalis. Enhancement of biofilm formation by P. gingivalis was only slightly reduced by inactivation of its autoinducer-2-producing gene luxS. CONCLUSION: The results suggest that P. gingivalis enhances biofilm formation by F. nucleatum by releasing diffusible signaling molecules other than autoinducer-2.
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    Diaz, P. I.; Zilm, P. S.; Rogers, A. H. Fusobacterium nucleatum supports the growth of Porphyromonas gingivalis in oxygenated and carbon-dioxide-depleted environments. Microbiology (London, U. K.) 2002, 148 (2), 467– 472,  DOI: 10.1099/00221287-148-2-467
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    Kolenbrander, P. E.; Palmer, R. J., Jr; Periasamy, S.; Jakubovics, N. S. Oral multispecies biofilm development and the key role of cell–cell distance. Nat. Rev. Microbiol. 2010, 8, 471,  DOI: 10.1038/nrmicro2381
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    Oral multispecies biofilm development and the key role of cell-cell distance
    Kolenbrander, Paul E.; Palmer, Robert J.; Periasamy, Saravanan; Jakubovics, Nicholas S.
    Nature Reviews Microbiology (2010), 8 (7), 471-480CODEN: NRMACK; ISSN:1740-1526. (Nature Publishing Group)
    Growth of oral bacteria in situ requires adhesion to a surface because the const. flow of host secretions thwarts the ability of planktonic cells to grow before they are swallowed. Therefore, oral bacteria evolved to form biofilms on hard tooth surfaces and on soft epithelial tissues, which often contain multiple bacterial species. Because these biofilms are easy to study, they have become the paradigm of multispecies biofilms. In this Review we describe the factors involved in the formation of these biofilms, including the initial adherence to the oral tissues and teeth, cooperation between bacterial species in the biofilm, signalling between the bacteria and its role in pathogenesis, and the transfer of DNA between bacteria. In all these aspects distance between cells of different species is integral for oral biofilm growth.
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    Mira, A. Oral microbiome studies: potential diagnostic and therapeutic implications. Adv. Dent. Res. 2018, 29, 71– 77,  DOI: 10.1177/0022034517737024
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    Oral Microbiome Studies: Potential Diagnostic and Therapeutic Implications
    Mira A
    Advances in dental research (2018), 29 (1), 71-77 ISSN:.
    Understanding the microbiology of dental caries is not a mere academic exercise; it provides the basis for preventive, diagnostic, and treatment strategies and gives the dentist a theoretical framework to become a better professional. The last years have seen the development of new research methodologies, ranging from high-throughput sequencing or "omics" techniques to new fluorescence microscopy applications and microfluidics, which have allowed the study of the oral microbiome to an unprecedented level of detail. Those studies have provided new insights about oral biofilm formation, biomarkers of caries risk, microbial etiology, appropriate sampling, identification of health-associated bacteria, and new anticaries strategies, among others. Several pitfalls are associated with the new technologies, including a small number of samples per study group, elevated cost, and genus- or species-based analyses that do not take into consideration intraspecies variability. However, the new data strongly suggest that saliva may not be an appropriate sample for etiological studies or for bacterial caries-risk tests, that microbial composition alone may be insufficient to predict caries risk, and that antimicrobial or immunization strategies targeting single species are unlikely to be effective. Strategies directed toward modulation of the oral biofilm, such as pre- and probiotics, emerge as promising new approaches to prevent tooth decay.
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    Labrecque, J.; Bodet, C.; Chandad, F.; Grenier, D. Effects of a high-molecular-weight cranberry fraction on growth, biofilm formation and adherence of Porphyromonas gingivalis. J. Antimicrob. Chemother. 2006, 58 (2), 439– 443,  DOI: 10.1093/jac/dkl220
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    Effects of a high-molecular-weight cranberry fraction on growth, biofilm formation and adherence of Porphyromonas gingivalis
    Labrecque, Julie; Bodet, Charles; Chandad, Fatiha; Grenier, Daniel
    Journal of Antimicrobial Chemotherapy (2006), 58 (2), 439-443CODEN: JACHDX; ISSN:0305-7453. (Oxford University Press)
    Porphyromonas gingivalis is a major etiol. agent of periodontitis, a destructive disease affecting the tooth-supporting tissues. Recent reports have indicated that high-mol.-wt. mols. from cranberry juice conc. can prevent the attachment of human pathogens to host tissues. The aim of the present study was to investigate the effect of non-dialysable material (NDM) prepd. from cranberry juice conc. on growth, biofilm formation and adherence properties of P. gingivalis. The effect of cranberry NDM on biofilm formation was studied using a polystyrene microplate assay and by SEM. The effect of cranberry NDM on the attachment properties of P. gingivalis was evaluated by a microplate assay in which mammalian proteins were immobilized into wells. Our results indicated that cranberry NDM is a potent inhibitor of biofilm formation by P. gingivalis. However, it has no effect on growth and viability of bacteria. Cranberry NDM also prevented significantly the attachment of P. gingivalis to surfaces coated with type I collagen, fibrinogen or human serum. Our data suggest that cranberry constituents may have a beneficial effect for the prevention and treatment of periodontitis by reducing the capacity of P. gingivalis to colonize periodontal sites.
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    La, V. D.; Howell, A. B.; Grenier, D. Anti-Porphyromonas gingivalis and anti-inflammatory activities of A-type cranberry proanthocyanidins. Antimicrob. Agents Chemother. 2010, 54 (5), 1778– 84,  DOI: 10.1128/AAC.01432-09
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    Silva, A. P.; Goncalves, R. S.; Borges, A. F.; Bedran-Russo, A. K.; Shinohara, M. S. Effectiveness of plant-derived proanthocyanidins on demineralization on enamel and dentin under artificial cariogenic challenge. Journal of applied oral science: revista FOB 2015, 23 (3), 302– 9,  DOI: 10.1590/1678-775720140304
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    Effectiveness of plant-derived proanthocyanidins on demineralization on enamel and dentin under artificial cariogenic challenge
    Silva Ana Paula Pereira da; Shinohara Mirela Sanae; Goncalves Rafael Simoes; Borges Ana Flavia Sanches; Bedran-Russo Ana Karina
    Journal of applied oral science : revista FOB (2015), 23 (3), 302-9 ISSN:.
    UNLABELLED: Dental caries is considered a disease of high prevalence and a constant problem in public health. Proanthocyanidins (PAs) are substances that have been the target of recent studies aiming to control or treat caries. OBJECTIVE: The aim of this in vitro study was to evaluate the efficacy of a treatment with grape seed extract, under cariogenic challenge, to minimize or even prevent the onset of caries in the enamel and dentin. MATERIAL AND METHODS: Blocks of enamel and dentin (6.0x6.0 mm) were obtained from bovine central incisors, polished, and selected by analysis of surface microhardness (SH). The blocks were randomly divided into 3 groups (n=15), according to the following treatments: GC (control), GSE (grape seed extract), GF (fluoride - 1,000 ppm). The blocks were subjected to 6 daily pH cycles for 8 days. Within the daily cycling, the specimens were stored in buffered solution. The blocks were then analyzed for perpendicular and surface hardness and polarized light microscopy. RESULTS: The means were subjected to statistical analysis using the ANOVA and Fisher's PLSD tests (p<0.05). For enamel SH, GF showed the highest hardness values. In the dentin, GF was also the one that showed higher hardness values, followed by GSE. Regarding the cross-sectional hardness values, all groups behaved similarly in both the enamel and dentin. The samples that were treated with GSE and fluoride (GF) showed statistically higher values than the control. CONCLUSION: Based on the data obtained in this in vitro study, it is suggested that grape seed extract inhibits demineralization of artificial carious lesions in both the enamel and dentin, but in a different scale in each structure and in a smaller scale when compared to fluoride.
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    Park, H.-J.; Jeong, S.-K.; Kim, S.-R.; Bae, S.-K.; Kim, W.-S.; Jin, S.-D.; Koo, T. H.; Jang, H.-O.; Yun, I.; Kim, K.-W.; Bae, M.-K. Resveratrol inhibits Porphyromonas gingivalis lipopolysaccharide-induced endothelial adhesion molecule expression by suppressing NF-κB activation. Arch. Pharmacal Res. 2009, 32 (4), 583– 591,  DOI: 10.1007/s12272-009-1415-7
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    Resveratrol inhibits Porphyromonas gingivalis lipopolysaccharide-induced endothelial adhesion molecule expression by suppressing NF-κB activation
    Park, Hyun-Joo; Jeong, Seong-Kyoon; Kim, Su-Ryun; Bae, Soo-Kyung; Kim, Woo-Sik; Jin, Seong-Deok; Koo, Tae Hyeon; Jang, Hye-Ock; Yun, Il; Kim, Kyu-Won; Bae, Moon-Kyoung
    Archives of Pharmacal Research (2009), 32 (4), 583-591CODEN: APHRDQ; ISSN:0253-6269. (Pharmaceutical Society of Korea)
    P. gingivalis is a major pathogen that is involved in the onset and progression of periodontal disease. This study investigated the effect of resveratrol, a naturally occurring polyphenol, on P. gingivalis LPS-accelerated vascular inflammation, a key step in the progression of periodontitis. Resveratrol significantly inhibited the P. gingivalis LPS-induced adhesion of leukocytes to endothelial cells and to the aortic endothelium by down-regulating the cell adhesion mols., ICAM-1 and VCAM-1. Moreover, the inhibition of the P. gingivalis LPS-induced cell adhesion mols. by resveratrol was mainly mediated by nuclear factor-κB (NF-κB). Resveratrol suppressed P. gingivalis LPS-stimulated IκBα phosphorylation and nuclear translocation of the p65 subunit of NF-κB in HMECs. Overall, these findings suggest that resveratrol significantly attenuates the P. gingivalis LPS-induced monocyte adhesion to the endothelium by suppressing the expression of the NF-κB-dependent cell adhesion mols., suggesting its therapeutic role in periodontal pathogen-induced vascular inflammation.
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    Minagawa, T.; Okui, T.; Takahashi, N.; Nakajima, T.; Tabeta, K.; Murakami, S.; Yamazaki, K. Resveratrol suppresses the inflammatory responses of human gingival epithelial cells in a SIRT1 independent manner. J. Periodontal Res. 2015, 50 (5), 586– 593,  DOI: 10.1111/jre.12238
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    Resveratrol suppresses the inflammatory responses of human gingival epithelial cells in a SIRT1 independent manner
    Minagawa, T.; Okui, T.; Takahashi, N.; Nakajima, T.; Tabeta, K.; Murakami, S.; Yamazaki, K.
    Journal of Periodontal Research (2015), 50 (5), 586-593CODEN: JPDRAY; ISSN:0022-3484. (Wiley-Blackwell)
    Background and Objective : In periodontitis, chronic infection by periodontopathic bacteria induces uncontrolled inflammation, which leads to periodontal tissue destruction. Human gingival epithelial cells (HGECs) constitute a crit. first line of defense against periodontopathic bacteria, both as a phys. barrier and as regulators of inflammation. Resveratrol, a polyphenol found in grapes and red wine, reportedly has anti-inflammatory properties. Therefore, we investigated the effects of resveratrol on the Porphyromonas gingivalis-induced inflammatory responses of HGECs and their mechanism. Material and Methods : We stimulated the HGEC line, epi 4, with live or heat-killed P. gingivalis in the presence of resveratrol, and analyzed expressions of the interleukin-8, monocyte chemoattractant protein-1 and interleukin-1β genes. We detd. the involvement of SIRT1 in the effect of resveratrol using sirtinol (a SIRT1 inhibitor) or SIRT1 knockdown. We also examd. whether the effects were mediated by activation of AMP-activated kinase, suppression of reactive oxygen species, or inhibition of nuclear factor-κB (NF-κB). Results : Resveratrol treatment decreased the expression of inflammatory cytokines and slightly increased the expression of SIRT1. However, neither SIRT1 inhibition nor SIRT1 knockdown counteracted its anti-inflammatory effects. Although resveratrol did not affect AMP-activated kinase activation or reactive oxygen species prodn., it slightly suppressed NF-κB translocation when cells were stimulated with heat-killed P. gingivalis. Conclusion : Resveratrol suppressed the inflammatory responses of P. gingivalis-stimulated HGECs, probably by inhibiting NF-κB signaling but independent of SIRT1.
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    Sakanaka, S.; Aizawa, M.; Kim, M.; Yamamoto, T. Inhibitory Effects of Green Tea Polyphenols on Growth and Cellular Adherence of an Oral Bacterium, Porphyromonas gingivalis. Biosci., Biotechnol., Biochem. 1996, 60 (5), 745– 749,  DOI: 10.1271/bbb.60.745
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    Kline, K. A.; Fälker, S.; Dahlberg, S.; Normark, S.; Henriques-Normark, B. Bacterial Adhesins in Host-Microbe Interactions. Cell Host Microbe 2009, 5 (6), 580– 592,  DOI: 10.1016/j.chom.2009.05.011
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    Bacterial adhesins in host-microbe interactions
    Kline, Kimberly A.; Faelker, Stefan; Dahlberg, Sofia; Normark, Staffan; Henriques-Normark, Birgitta
    Cell Host & Microbe (2009), 5 (6), 580-592CODEN: CHMECB; ISSN:1931-3128. (Cell Press)
    A review. Most commensal and pathogenic bacteria interacting with eukaryotic hosts express adhesive mols. on their surfaces that promote interaction with host cell receptors or with sol. macromols. Even though bacterial attachment to epithelial cells may be beneficial for bacterial colonization, adhesion may come at a cost because bacterial attachment to immune cells can facilitate phagocytosis and clearing. Many pathogenic bacteria have solved this dilemma by producing an antiphagocytic surface layer usually consisting of polysaccharide and by expressing their adhesins on polymeric structures that extend out from the cell surface. In this review, we will focus on the interaction between bacterial adhesins and the host, with an emphasis on pilus-like structures.
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    González de Llano, D.; Gil-Sánchez, I.; Esteban-Fernández, A.; Ramos, A. M.; Fernández-Díaz, M.; Cueva, C.; Moreno-Arribas, M. V.; Bartolomé, B. Reciprocal beneficial effects between wine polyphenols and probiotics: an exploratory study. Eur. Food Res. Technol. 2017, 243 (3), 531– 538,  DOI: 10.1007/s00217-016-2770-5
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    Garcia-Ruiz, A.; Gonzalez de Llano, D.; Esteban-Fernandez, A.; Requena, T.; Bartolome, B.; Moreno-Arribas, M. V. Assessment of probiotic properties in lactic acid bacteria isolated from wine. Food Microbiol. 2014, 44, 220– 5,  DOI: 10.1016/j.fm.2014.06.015
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    Assessment of probiotic properties in lactic acid bacteria isolated from wine
    Garcia-Ruiz, Almudena; Gonzalez de Llano, Dolores; Esteban-Fernandez, Adelaida; Requena, Teresa; Bartolome, Begona; Moreno-Arribas, M. Victoria
    Food Microbiology (2014), 44 (), 220-225CODEN: FOMIE5; ISSN:0740-0020. (Elsevier Ltd.)
    Probiotic properties are highly strain-dependent but rarely studied in enol. lactic acid bacteria (LAB). In this study, the probiotic features of 11 strains of Lactobacillus spp., Pediococcus spp., and Oenococcus oeni, including saliva and acid resistance, bile tolerance and exopolysaccharides' prodn., were investigated. The assays included two probiotic ref. strains (Lactobacillus plantarum CLC 17 and Lactobacillus fermentum CECT5716). The Lactobacillus and Pediococcus strains showed high resistance to lysozyme (>80% resistance to 100 mg/L of lysozyme under conditions simulating the in vivo diln. by saliva) and were capable of surviving at low pH values (pH 1.8) and bile salts, suggesting good adaptation of the wine strains to gastrointestinal conditions. The ability of the strains to adhere to the intestinal mucosa and the inhibition of the adhesion of Escherichia coli to human intestinal cells were also evaluated. Adhesion levels of enol. LAB to Caco-2 cells varied from 0.37% to 12.2%, depending on the strain. In particular, Pediococcus pentosaceus CIAL-86 showed a high percentage of adhesion to intestinal cells (>12%), even higher than that shown by the probiotic ref. strains, and a high anti-adhesion activity against E. coli CIAL-153 (>30%), all of which support this wine LAB strain as a potential probiotic.
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    Pereira-Caro, G.; Oliver, C. M.; Weerakkody, R.; Singh, T.; Conlon, M.; Borges, G.; Sanguansri, L.; Lockett, T.; Roberts, S. A.; Crozier, A.; Augustin, M. A. Chronic administration of a microencapsulated probiotic enhances the bioavailability of orange juice flavanones in humans. Free Radical Biol. Med. 2015, 84, 206– 14,  DOI: 10.1016/j.freeradbiomed.2015.03.010
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    Chronic administration of a microencapsulated probiotic enhances the bioavailability of orange juice flavanones in humans
    Pereira-Caro, Gema; Oliver, Christine M.; Weerakkody, Rangika; Singh, Tanoj; Conlon, Michael; Borges, Gina; Sanguansri, Luz; Lockett, Trevor; Roberts, Susan A.; Crozier, Alan; Augustin, Mary Ann
    Free Radical Biology & Medicine (2015), 84 (), 206-214CODEN: FRBMEH; ISSN:0891-5849. (Elsevier B.V.)
    Orange juice (OJ) flavanones are bioactive polyphenols that are absorbed principally in the large intestine. Ingestion of probiotics has been assocd. with favorable changes in the colonic microflora. The present study examd. the acute and chronic effects of orally administered Bifidobacterium longum R0175 on the colonic microflora and bioavailability of OJ flavanones in healthy volunteers. In an acute study volunteers drank OJ with and without the microencapsulated probiotic, whereas the chronic effects were examd. when OJ was consumed after daily supplementation with the probiotic over 4 wk. Bioavailability, assessed by 0-24 h urinary excretion, was similar when OJ was consumed with and without acute probiotic intake. Hesperetin-O-glucuronides, naringenin-O-glucuronides, and hesperetin-3'-O-sulfate were the main urinary flavanone metabolites. The overall urinary excretion of these metabolites after OJ ingestion and acute probiotic intake corresponded to 22% of intake, whereas excretion of key colon-derived phenolic and arom. acids was equiv. to 21% of the ingested OJ (poly)phenols. Acute OJ consumption after chronic probiotic intake over 4 wk resulted in the excretion of 27% of flavanone intake, and excretion of selected phenolic acids also increased significantly to 43% of (poly)phenol intake, corresponding to an overall bioavailability of 70%. Neither the probiotic bacterial profiles of stools nor the stool moisture, wt., pH, or levels of short-chain fatty acids and phenols differed significantly between treatments. These findings highlight the pos. effect of chronic, but not acute, intake of microencapsulated B. longum R0175 on the bioavailability of OJ flavanones.
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    Faria, A.; Fernandes, I.; Norberto, S.; Mateus, N.; Calhau, C. Interplay between anthocyanins and gut microbiota. J. Agric. Food Chem. 2014, 62 (29), 6898– 902,  DOI: 10.1021/jf501808a
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    Interplay between Anthocyanins and Gut Microbiota
    Faria, Ana; Fernandes, Iva; Norberto, Sonia; Mateus, Nuno; Calhau, Conceicao
    Journal of Agricultural and Food Chemistry (2014), 62 (29), 6898-6902CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
    A review. Anthocyanins are naturally occurring compds. abundant in the human diet. Evidence has accumulated regarding the pos. assocn. of their intake with healthy biol. effects. The microbiota has just been started to be considered as a metabolic organ, hence contributing to the metab. of phenolic compds. and, consequently, to their bioavailability and the biol. effects displayed by them. This review aimed to compile information regarding interaction of anthocyanins with the microbiota, from two perspectives: (i) identification of their colonic metabolites as potential bioactive mols. and (ii) their role as prebiotic agents. These perspectives are key points in anthocyanin metabolomics. Several metabolites have been identified after anthocyanin consumption with potential health benefits, in particular phenolic acids and simple phenols. On the other hand, microbiota modulation is closely related to several physiol. impairments, and its modulation has been considered as a possible mechanism by which phenolic compds. may exert their effect.
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    Walle, T.; Browning, A. M.; Steed, L. L.; Reed, S. G.; Walle, U. K. Flavonoid glucosides are hydrolyzed and thus activated in the oral cavity in humans. J. Nutr. 2005, 135 (1), 48– 52,  DOI: 10.1093/jn/135.1.48
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    Flavonoid glucosides are hydrolyzed and thus activated in the oral cavity in humans
    Walle, Thomas; Browning, Alyson M.; Steed, Lisa L.; Reed, Susan G.; Walle, U. Kristina
    Journal of Nutrition (2005), 135 (1), 48-52CODEN: JONUAI; ISSN:0022-3166. (American Society for Nutritional Sciences)
    Increasing epidemiol. evidence supports the view that dietary flavonoids have protective roles in oral diseases, including cancer. However, the dietary forms of flavonoids, the flavonoid glycosides, must first be hydrolyzed to the aglycons, which is thought to occur mainly in the intestine. In the present study we tested whether this hydrolytic activity occurs in the oral cavity. Saliva was collected from human subjects, incubated with flavonoid glycosides, and analyzed for aglycon formation by HPLC. When quercetin 4'-glucoside or genistein 7-glucoside was incubated with human saliva, hydrolysis to quercetin and genistein, resp., was detected within minutes. Studies of addnl. flavonoid glycosides demonstrated that glucose conjugates were rapidly hydrolyzed, but not conjugates with other sugars, i.e., rutin, quercitrin, and naringin. In a limited study of 17 subjects, the interindividual variability in the hydrolysis of genistein 7-glucoside was >20-fold. This supports the contention that salivary hydrolysis of certain flavonoid glucosides may be important in some individuals but not in others. Support for a bacterial contribution to this hydrolysis was obtained from the inhibitory effect of antibacterials in vivo and in vitro and from expts. with subcultured oral bacterial colonies. However, cytosol isolated from oral epithelial cells was also capable of effective hydrolysis. Dietary flavonoid glucosides may thus be hydrolyzed in the oral cavity by both bacteria and shedded epithelial cells to deliver the biol. active aglycons at the surface of the epithelial cells. The aglycons quercetin and genistein both potently inhibited proliferation of oral cancer cells. The large interindividual variability in this hydrolytic activity may be a factor that should be taken into consideration in future studies.
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    Muñoz-Gonzalez, C.; Cueva, C.; Angeles Pozo-Bayon, M.; Victoria Moreno-Arribas, M. Ability of human oral microbiota to produce wine odorant aglycones from odourless grape glycosidic aroma precursors. Food Chem. 2015, 187, 112– 9,  DOI: 10.1016/j.foodchem.2015.04.068
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    Cueva, C.; Sanchez-Patan, F.; Monagas, M.; Walton, G. E.; Gibson, G. R.; Martin-Alvarez, P. J.; Bartolome, B.; Moreno-Arribas, M. V. In vitro fermentation of grape seed flavan-3-ol fractions by human faecal microbiota: changes in microbial groups and phenolic metabolites. FEMS Microbiol. Ecol. 2013, 83 (3), 792– 805,  DOI: 10.1111/1574-6941.12037
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    In vitro fermentation of grape seed flavan-3-ol fractions by human faecal microbiota: changes in microbial groups and phenolic metabolites
    Cueva, Carolina; Sanchez-Patan, Fernando; Monagas, Maria; Walton, Gemma E.; Gibson, Glenn R.; Martin-Alvarez, Pedro J.; Bartolome, Begona; Moreno-Arribas, M. Victoria
    FEMS Microbiology Ecology (2013), 83 (3), 792-805CODEN: FMECEZ; ISSN:0168-6496. (Wiley-Blackwell)
    With the aim of investigating the potential of flavan-3-ols to influence the growth of intestinal bacterial groups, we have carried out the in vitro fermn., with human faecal microbiota, of two purified fractions from grape seed ext. (GSE): GSE-M (70% monomers and 28% procyanidins) and GSE-O (21% monomers and 78% procyanidins). Samples were collected at 0, 5, 10, 24, 30 and 48 h of fermn. for bacterial enumeration by fluorescent in situ hybridization and for anal. of phenolic metabolites. Both GSE-M and GSE-O fractions promoted growth of Lactobacillus/Enterococcus and decrease in the Clostridium histolyticum group during fermn., although the effects were only statistically significant with GSE-M for Lactobacillus/Enterococcus (at 5 and 10 h of fermn.) and GSE-O for C. histolyticum (at 10 h of fermn.). Main changes in polyphenol catabolism also occurred during the first 10 h of fermn.; however, no significant correlation coeffs. (P > 0.05) were found between changes in microbial populations and precursor flavan-3-ols or microbial metabolites. Together, these data suggest that the flavan-3-ol profile of a particular food source could affect the microbiota compn. and its catabolic activity, inducing changes that could in turn affect the bioavailability and potential bioactivity of these compds.
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  • Abstract

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    Figure 1

    Figure 1. Cellular viability of HGF-1 fibroblasts in the presence of phenolic compounds and extracts (10 and 50 μg/mL) after 30 min and 24 h incubations. Results are expressed as media of three independent assays ± standard deviation.

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    Figure 2

    Figure 2. Adherence inhibition (%) of oral pathogens (A) S. mutans, (B) F. nucleatum, and (C) P. gingivalis) by phenolic compounds and extracts (10 and 50 μg/mL). Results are expressed as the media of three independent assays ± standard error. * indicates p < 0.05, ** indicates p < 0.01, and *** indicated p < 0.001.

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    Figure 3

    Figure 3. Percentage (%) of exclusion, displacement and competition of S. mutans adherence by S. dentisani probiotic strain 7746 and polyphenols. Results are expressed as the media of three independent experiments ± standard error. Data were analyzed by two-way ANOVA and Bonferroni test. * indicates p < 0.05.

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  • References

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    This article references 60 other publications.

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      Over the last few decades, polyphenols, and flavonoids in particular, have attracted the interest of researchers, as they have been assocd. with the health-promoting effects derived from diets rich in vegetables and fruits, including moderate wine consumption. Recent scientific evidence suggests that wine polyphenols exert their effects through interactions with the gut microbiota, as they seem to modulate microbiota and, at the same time, are metabolized by intestinal bacteria into specific bioavailable metabolites. Microbial metabolites are better absorbed than their precursors and may be responsible for pos. health activities in the digestive system (local effects) and, after being absorbed, in tissues and organs (systemic effects). Differences in gut microbiota compn. and functionality among individuals can affect polyphenol activity and, therefore, their health effects. The aim of this review is to integrate the understanding of the metab. and mechanisms of action of wine polyphenols at both local and systemic levels, underlining their impact on the gut microbiome and the inter-individual variability assocd. with polyphenols metab. and further physiol. effects. The advent of promising dietary approaches linked to wine polyphenols beyond the gut microbiota community and metab. are also discussed.
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      BACKGROUND Observational cohort studies and a secondary prevention trial have shown an inverse assocn. between adherence to the Mediterranean diet and cardiovascular risk. We conducted a randomized trial of this diet pattern for the primary prevention of cardiovascular events. METHODS In a multicenter trial in Spain, we randomly assigned participants who were at high cardiovascular risk, but with no cardiovascular disease at enrollment, to one of three diets: a Mediterranean diet supplemented with extra-virgin olive oil, a Mediterranean diet supplemented with mixed nuts, or a control diet (advice to reduce dietary fat). Participants received quarterly individual and group educational sessions and, depending on group assignment, free provision of extra-virgin olive oil, mixed nuts, or small nonfood gifts. The primary end point was the rate of major cardiovascular events (myocardial infarction, stroke, or death from cardiovascular causes). On the basis of the results of an interim anal., the trial was stopped after a median follow-up of 4.8 years. RESULTS A total of 7447 persons were enrolled (age range, 55 to 80 years); 57% were women. The two Mediterranean-diet groups had good adherence to the intervention, according to self-reported intake and biomarker analyses. A primary end-point event occurred in 288 participants. The multivariable-adjusted hazard ratios were 0.70 (95% confidence interval [CI], 0.54 to 0.92) and 0.72 (95% CI, 0.54 to 0.96) for the group assigned to a Mediterranean diet with extra-virgin olive oil (96 events) and the group assigned to a Mediterranean diet with nuts (83 events), resp., vs. the control group (109 events). No diet-related adverse effects were reported. CONCLUSIONS Among persons at high cardiovascular risk, a Mediterranean diet supplemented with extra-virgin olive oil or nuts reduced the incidence of major cardiovascular events.
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      Vázquez-Fresno, R.; Llorach, R.; Urpi-Sarda, M.; Khymenets, O.; Bulló, M.; Corella, D.; Fitó, M.; Martínez-González, M. A.; Estruch, R.; Andres-Lacueva, C. An NMR metabolomics approach reveals a combined-biomarkers model in a wine interventional trial with validation in free-living individuals of the PREDIMED study. Metabolomics 2015, 11 (4), 797– 806,  DOI: 10.1007/s11306-014-0735-x
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      The development of robust biomarkers of consumption would improve the classification of participants with regard to their dietary exposure. In addn., validation of them in free-living individuals remains an important challenge. The aim of this study is to assess wine intake biomarkers using an NMR metabolomic approach to measure the utility of these biomarkers in a wine interventional study (WIS, n = 56) and also to evaluate them in a free-living individuals (PREDIMED study, n = 91). Nine metabolites showed a significantly higher presence in urinary excretion in WIS after wine intake: five food metabolome metabolites (tartrate, Et glucuronide [EtG], 2,3-butanediol, mannitol, and ethanol); one related to the endogenous response to wine exposure (3-methyl-2-oxovalerate) and three unidentified compds. Receiver operating characteristic (ROC) curve for each single metabolite were evaluated and exhibited areas under the curves (AUC) between 67.4 and 86.3 % when they were evaluated individually. Then, a logistic regression model was fitted to generate a combined-biomarkers model using these metabolites. The model generated which included tartrate-EtG, showed an AUC of 90.7 % in WIS. Similarly, the AUC in the PREDIMED study was 92.4 %. Results showed that a model combining tartrate-EtG is more useful for evaluating exposure to wine than single biomarkers, both in interventional studies and epidemiol. data. To our knowledge, this is the first time that a combined-biomarker model using an NMR platform in wine biomarkers' research has been generated and reproduced in a free-living population.
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      Queipo-Ortuno, M. I.; Boto-Ordonez, M.; Murri, M.; Gomez-Zumaquero, J. M.; Clemente-Postigo, M.; Estruch, R.; Cardona Diaz, F.; Andres-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 (6), 1323– 34,  DOI: 10.3945/ajcn.111.027847
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      Background: Few studies have investigated the effect of dietary polyphenols on the complex human gut microbiota, and they focused mainly on single polyphenol mols. and select bacterial populations. Objective: The objective was to evaluate the effect of a moderate intake of red wine polyphenols on select gut microbial groups implicated in host health benefits. Design: Ten healthy male volunteers underwent a randomized, crossover, controlled intervention study. After a washout period, all of the subjects received red wine, the equiv. amt. of de-alcoholized red wine, or gin for 20 d each. Total fecal DNA was submitted to polymerase chain reaction (PCR)-denaturing gradient gel electrophoresis and real-time quant. PCR to monitor and quantify changes in fecal microbiota. Several biochem. markers were measured. Results: The dominant bacterial compn. did not remain const. over the different intake periods. Compared with baseline, the daily consumption of red wine polyphenol for 4 wk significantly increased the no. of Enterococcus, Prevotella, Bacteroides, Bifidobacterium, Bacteroides uniformis, Eggerthella lenta, and Blautia coccoides-Eubacterium rectale groups (P < 0.05). In parallel, systolic and diastolic blood pressures and triglyceride, total cholesterol, HDL cholesterol, and C-reactive protein concns. decreased significantly (P < 0.05). Moreover, changes in cholesterol and C-reactive protein concns. were linked to changes in the bifidobacteria no. Conclusion: This study showed that red wine consumption can significantly modulate the growth of select gut microbiota in humans, which suggests possible prebiotic benefits assocd. with the inclusion of red wine polyphenols in the diet.
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      Moreno-Indias, I.; Sanchez-Alcoholado, L.; Perez-Martinez, P.; Andres-Lacueva, C.; Cardona, F.; Tinahones, F.; Queipo-Ortuno, M. I. Red wine polyphenols modulate fecal microbiota and reduce markers of the metabolic syndrome in obese patients. Food Funct. 2016, 7 (4), 1775– 1787,  DOI: 10.1039/C5FO00886G
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      Red wine polyphenols modulate fecal microbiota and reduce markers of the metabolic syndrome in obese patients
      Moreno-Indias Isabel; Cardona Fernando; Tinahones Francisco; Queipo-Ortuno Maria Isabel; Sanchez-Alcoholado Lidia; Perez-Martinez Pablo; Andres-Lacueva Cristina
      Food & function (2016), 7 (4), 1775-87 ISSN:.
      This study evaluated the possible prebiotic effect of a moderate intake of red wine polyphenols on the modulation of the gut microbiota composition and the improvement in the risk factors for the metabolic syndrome in obese patients. Ten metabolic syndrome patients and ten healthy subjects were included in a randomized, crossover, controlled intervention study. After a washout period, the subjects consumed red wine and de-alcoholized red wine over a 30 day period for each. The dominant bacterial composition did not differ significantly between the study groups after the two red wine intake periods. In the metabolic syndrome patients, red wine polyphenols significantly increased the number of fecal bifidobacteria and Lactobacillus (intestinal barrier protectors) and butyrate-producing bacteria (Faecalibacterium prausnitzii and Roseburia) at the expense of less desirable groups of bacteria such as LPS producers (Escherichia coli and Enterobacter cloacae). The changes in gut microbiota in these patients could be responsible for the improvement in the metabolic syndrome markers. Modulation of the gut microbiota by using red wine could be an effective strategy for managing metabolic diseases associated with obesity.
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    7. 7
      Barroso, E.; Munoz-Gonzalez, I.; Jimenez, E.; Bartolome, B.; Moreno-Arribas, M. V.; Pelaez, C.; Del Carmen Martinez-Cuesta, M.; Requena, T. Phylogenetic profile of gut microbiota in healthy adults after moderate intake of red wine. Mol. Nutr. Food Res. 2017, 61 (3), 1600620,  DOI: 10.1002/mnfr.201600620
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      Palmer, R. J., Jr. Composition and development of oral bacterial communities. Periodontol. 2000 2014, 64 (1), 20– 39,  DOI: 10.1111/j.1600-0757.2012.00453.x
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      Composition and development of oral bacterial communities
      Palmer Robert J Jr
      Periodontology 2000 (2014), 64 (1), 20-39 ISSN:.
      The oral bacterial microbiome encompasses approximately 700 commonly occurring phylotypes, approximately half of which can be present at any time in any individual. These bacteria are largely indigenous to the oral cavity; this limited habitat range suggests that interactions between the various phylotypes, and between the phylotypes and their environment, are crucial for their existence. Molecular cataloging has confirmed many basic observations on the composition of the oral microbiome that were formulated well before ribosomal RNA-based systematics, but the power and the scope of molecular taxonomy have resulted in the discovery of new phylotypes and, more importantly, have made possible a level of bacterial community analysis that was unachievable with classical methods. Bacterial community structure varies with location within the mouth, and changes in community structure are related to disease initiation and disease progression. Factors that influence the formation and the evolution of communities include selective adherence to epithelial or tooth surfaces, specific cell-to-cell binding as a driver of early community composition, and interorganismal interaction leading to alteration of the local environment, which represents the first step on the road to oral disease. A comprehensive understanding of how these factors interact to drive changes in the composition of the oral microbial community can lead to new strategies for the inhibition of periodontal diseases and dental caries.
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      Marsh, P. D.; Bradshaw, D. J. Dental plaque as a biofilm. J. Ind. Microbiol. 1995, 15 (3), 169– 75,  DOI: 10.1007/BF01569822
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      Dental plaque as a biofilm
      Marsh, P. D.; Bradshaw, D. J.
      Journal of Industrial Microbiology (1995), 15 (3), 169-75CODEN: JIMIE7; ISSN:0169-4146. (Macmillan Scientific & Medical Division)
      A review with 62 refs. Dental plaque is the diverse microbial community found on the tooth surface embedded in a matrix of polymers of bacterial and salivary origin. Once a tooth surface is cleaned, a conditioning film of proteins and glycoproteins is adsorbed rapidly to the tooth surface. Plaque formation involves the interaction between early bacterial colonizers and this film (the acquired enamel pellicle). To facilitate colonization of the tooth surface, some receptors on salivary mols. are only exposed to bacteria once the mol. is adsorbed to a surface. Subsequently, secondary colonizers adhere to the already attached early colonizers (co-aggregation) through specific mol. interactions. These can involve protein-protein or carbohydrate-protein (lectin) interactions, and this process contributes to detg. the pattern of bacterial succession. As the biofilm develops, gradients in biol. significant factors develop, and these permit the co-existence of species that would be incompatible with each other in a homogeneous environment. Dental plaque develops naturally, but it also assocd. with two of the most prevalent diseases affecting industrialized societies (caries and periodontal diseases). Future strategies to control dental plaque will be targeted to interfering with the formation, structure and pattern of development of this biofilm.
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      Esteban-Fernández, A.; Zorraquín-Peña, I.; González de Llano, D.; Bartolomé, B.; Moreno-Arribas, M. V. The role of wine and food polyphenols in oral health. Trends Food Sci. Technol. 2017, 69 (Part A), 118– 130,  DOI: 10.1016/j.tifs.2017.09.008
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      The role of wine and food polyphenols in oral health
      Esteban-Fernandez, Adelaida; Zorraquin-Pena, Irene; Gonzalez de Llano, Dolores; Bartolome, Begona; Moreno-Arribas, M. Victoria
      Trends in Food Science & Technology (2017), 69 (Part_A), 118-130CODEN: TFTEEH; ISSN:0924-2244. (Elsevier Ltd.)
      A review. There is a growing interest in understanding the human oral microbiome, due to its important role in promoting health, as reported in a no. of studies. Several factors can affect the compn. of the oral microbiota (e.g. hygienic habits, genetics, environment ...). Among them, diet is one of the most significant external factors that modulate oral microbiota, thereby affecting the balance between host health and disease. Although the compn. of oral microbiota can be considered dynamic, there is an equil. between commensal bacteria and pathogens on which oral health status relies. This study emphasizes the alteration of the balance previously mentioned, when the pathogenic bacteria population increases to the detriment of beneficial commensal bacteria, which prompts microbial-derived oral diseases such as caries, gingivitis and periodontitis that may affect every human at some point in life. Dietary polyphenols and, in particular, wine polyphenols seem to modulate the compn. of the oral microbiota suggesting plausible benefits in the prevention of caries and periodontal diseases. However, at this point, knowledge is still preliminary, and more research needs to be conducted at different levels. This review focuses on the current research regarding polyphenols and their role in preventing microbial-derived oral diseases. It gives a holistic view that emphasizes the interactions of these bioactive compds. among oral pathogens as well as their potential metab. by oral bacteria.
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      Takahashi, N.; Nyvad, B. The role of bacteria in the caries process: ecological perspectives. J. Dent. Res. 2011, 90 (3), 294– 303,  DOI: 10.1177/0022034510379602
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      The role of bacteria in the caries process: ecological perspectives
      Takahashi N; Nyvad B
      Journal of dental research (2011), 90 (3), 294-303 ISSN:.
      Dental biofilms produce acids from carbohydrates that result in caries. According to the extended caries ecological hypothesis, the caries process consists of 3 reversible stages. The microflora on clinically sound enamel surfaces contains mainly non-mutans streptococci and Actinomyces, in which acidification is mild and infrequent. This is compatible with equilibrium of the demineralization/remineralization balance or shifts the mineral balance toward net mineral gain (dynamic stability stage). When sugar is supplied frequently, acidification becomes moderate and frequent. This may enhance the acidogenicity and acidurance of the non-mutans bacteria adaptively. In addition, more aciduric strains, such as 'low-pH' non-mutans streptococci, may increase selectively. These microbial acid-induced adaptation and selection processes may, over time, shift the demineralization/remineralization balance toward net mineral loss, leading to initiation/progression of dental caries (acidogenic stage). Under severe and prolonged acidic conditions, more aciduric bacteria become dominant through acid-induced selection by temporary acid-impairment and acid-inhibition of growth (aciduric stage). At this stage, mutans streptococci and lactobacilli as well as aciduric strains of non-mutans streptococci, Actinomyces, bifidobacteria, and yeasts may become dominant. Many acidogenic and aciduric bacteria are involved in caries. Environmental acidification is the main determinant of the phenotypic and genotypic changes that occur in the microflora during caries.
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      Conrads, G. Oral anaerobes in health and disease. Anaerobe 2015, 35 (Pt A), 1– 2,  DOI: 10.1016/j.anaerobe.2015.05.011
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      Loesche, W. J. Microbiology of Dental Decay and Periodontal Disease. In Medical Microbiology, 4th ed.; Baron, S., Ed.; University of Texas Medical Branch at Galveston: Galveston, TX, 1996.
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      López-López, A.; Camelo-Castillo, A.; Ferrer, M. D.; Simon-Soro, Á.; Mira, A. Health-Associated Niche Inhabitants as Oral Probiotics: The Case of Streptococcus dentisani. Front. Microbiol. 2017, 8, 379,  DOI: 10.3389/fmicb.2017.00379
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      Health-Associated Niche Inhabitants as Oral Probiotics: The Case of Streptococcus dentisani
      Lopez-Lopez Arantxa; Camelo-Castillo Anny; Ferrer Maria D; Simon-Soro Aurea; Mira Alex
      Frontiers in microbiology (2017), 8 (), 379 ISSN:1664-302X.
      Oral diseases, including dental caries and periodontitis, are among the most prevalent diseases worldwide and develop as a consequence of a microbial dysbiosis. Several bacterial strains are being tested as potential oral health-promoting organisms, but usually they are species isolated from niches other than the site where they must exert its probiotic action, typically from fecal samples. We hypothesize that oral inhabitants associated to health conditions will be more effective than traditional, gut-associated probiotic species in key aspects such as colonization of the oral site where disease takes place or the possession of oral health promoting functions, as well as more practical issues like safety and toxicity, and establishing proper doses for administration. As an example of these active colonizers, we describe the case of Streptococcus dentisani, a new streptococcal species isolated from dental plaque of caries-free individuals. We have detected it in 98% of dental plaque samples from healthy individuals and, as expected, it does not produce any toxic secondary metabolite and does not survive a simulated stomach digestion, preventing potential secondary effects. Besides, this species has a double probiotic action, as it inhibits the growth of major oral pathogens through the production of bacteriocins, and also buffers acidic pH (the primary cause of dental caries) through an arginolytic pathway. We propose the use of S. dentisani as a promising probiotic against tooth decay.
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      Gupta, N. D.; Sharma, S.; Sharma, V. K. Probiotic – An emerging therapy in recolonizing periodontal pocket. Journal of Oral Biology and Craniofacial Research 2017, 7 (1), 72– 73,  DOI: 10.1016/j.jobcr.2016.09.002
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      Probiotic - An emerging therapy in recolonizing periodontal pocket
      Gupta N D; Sharma Shweta; Sharma Vivek Kumar
      Journal of oral biology and craniofacial research (2017), 7 (1), 72-73 ISSN:2212-4268.
      One of the etiological factors in the pathogenesis of periodontitis is reduction or the absence of the so-called "beneficial bacteria". Most of the globally applied treatment approach is based on subgingival bacterial elimination but recolonization with less pathogenic bacteria is seen within weeks. Therefore, researchers have started focusing on shifting the current treatment approach from specific bacterial elimination to restoring periodontal pocket with beneficial bacteria. This alteration in the ecology of niches from the one with the pathological plaque to the one with the biofilm of commensals can be achieved via subgingival application of probiotics. This article suggests the important prospects of subgingival delivery of probiotics in guiding periodontal recolonization with beneficial bacteria and emphasizes research in this study field.
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    16. 16
      Burton, J. P.; Wescombe, P. A.; Moore, C. J.; Chilcott, C. N.; Tagg, J. R. Safety Assessment of the Oral Cavity Probiotic Streptococcus salivarius K12. Appl. Environ. Microbiol. 2006, 72 (4), 3050– 3053,  DOI: 10.1128/AEM.72.4.3050-3053.2006
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      Monagas, M.; Urpi-Sarda, M.; Sanchez-Patan, F.; Llorach, R.; Garrido, I.; Gomez-Cordoves, C.; Andres-Lacueva, C.; Bartolome, B. Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites. Food Funct. 2010, 1 (3), 233– 53,  DOI: 10.1039/c0fo00132e
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      Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites
      Monagas, Maria; Urpi-Sarda, Mireia; Sanchez-Patan, Fernando; Llorach, Rafael; Garrido, Ignacio; Gomez-Cordoves, Carmen; Andres-Lacueva, Cristina; Bartolome, Begona
      Food & Function (2010), 1 (3), 233-253CODEN: FFOUAI; ISSN:2042-6496. (Royal Society of Chemistry)
      A review. Flavan-3-ols, occurring in monomeric, as well as in oligomeric and polymeric forms (also known as condensed tannins or proanthocyanidins), are among the most abundant and bioactive dietary polyphenols, but their in vivo health effects in humans may be limited because of their recognition as xenobiotics. Bioavailability of flavan-3-ols is largely influenced by their d.p.; while monomers are readily absorbed in the small intestine, oligomers and polymers need to be biotransformed by the colonic microbiota before absorption. Therefore, phenolic metabolites, rather than the original high mol. wt. compds. found in foods, may be responsible for the health effects derived from flavan-3-ol consumption. Flavan-3-ol phenolic metabolites differ in structure, amt. and excretion site. Phase II or tissular metabolites derived from the small intestine and hepatic metab. are presented as conjugated derivs. (glucuronic acid or sulfate esters, Me ether, or their combined forms) of monomeric flavan-3-ols and are preferentially eliminated in the bile, whereas microbial metabolites are rather simple conjugated lactones and phenolic acids that are largely excreted in urine. Although the colon is seen as an important organ for the metab. of flavan-3-ols, the microbial catabolic pathways of these compds. are still under consideration, partly due to the lack of identification of bacteria with such capacity. Studies performed with synthesized or isolated phase II conjugated metabolites have revealed that they could have an effect beyond their antioxidant properties, by interacting with signalling pathways implicated in important processes involved in the development of diseases, among other bioactivities. However, the biol. properties of microbe-derived metabolites in their actual conjugated forms remain largely unknown. Currently, there is an increasing interest in their effects on intestinal infections, inflammatory intestinal diseases and overall gut health. The present review will give an insight into the metab. and microbial biotransformation of flavan-3-ols, including tentative catabolic pathways and aspects related to the identification of bacteria with the ability to catabolize these kinds of polyphenols. Also, the in vitro bioactivities of phase II and microbial phenolic metabolites will be covered in detail.
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      Muñoz-González, I.; Thurnheer, T.; Bartolomé, B.; Moreno-Arribas, M. V. Red Wine and Oenological Extracts Display Antimicrobial Effects in an Oral Bacteria Biofilm Model. J. Agric. Food Chem. 2014, 62 (20), 4731– 4737,  DOI: 10.1021/jf501768p
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      Sánchez-Patán, F.; Cueva, C.; Monagas, M.; Walton, G. E.; Gibson M, G. R.; Quintanilla-López, J. E.; Lebrón-Aguilar, R.; Martín-Álvarez, P. J.; Moreno-Arribas, M. V.; Bartolomé, B. In Vitro Fermentation of a Red Wine Extract by Human Gut Microbiota: Changes in Microbial Groups and Formation of Phenolic Metabolites. J. Agric. Food Chem. 2012, 60 (9), 2136– 2147,  DOI: 10.1021/jf2040115
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      In vitro fermentation of a red wine extract by human gut microbiota: Changes in microbial groups and formation of phenolic metabolites
      Sanchez-Patan, Fernando; Cueva, Carolina; Monagas, Maria; Walton, Gemma E.; Gibson M., Glenn R.; Quintanilla-Lopez, Jesus E.; Lebron-Aguilar, Rosa; Martin-Alvarez, P. J.; Moreno-Arribas, M. Victoria; Bartolome, Begona
      Journal of Agricultural and Food Chemistry (2012), 60 (9), 2136-2147CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
      An in vitro batch culture fermn. expt. was conducted with fecal inocula from three healthy volunteers in the presence and absence of a red wine ext. Changes in main bacterial groups were detd. by FISH during a 48 h fermn. period. The catabolism of main flavonoids (i.e., flavan-3-ols and anthocyanins) and the formation of a wide a range of phenolic microbial metabolites were detd. by a targeted UPLC-PAD-ESI-TQ MS method. Statistical anal. revealed that catechol/pyrocatechol, as well as 4-hydroxy-5-(phenyl)-valeric, 3- and 4-hydroxyphenylacetic, phenylacetic, phenylpropionic, and benzoic acids, showed the greatest increases in concn. during fermn., whereas 5-(3'-hydroxyphenyl)-γ-valerolactone, its open form 4-hydroxy-5-(3'-hydroxyphenyl)-valeric acid, and 3,4-dihydroxyphenylacetic acid represented the largest interindividual variations in the catabolism of red wine polyphenols. Despite these changes, microbial catabolism did not produce significant changes in the main bacterial groups detected, although a slight inhibition of the Clostridium histolyticum group was obsd.
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    20. 20
      Sánchez-Patán, F.; Cueva, C.; Monagas, M.; Walton, G. E.; Gibson, G. R.; Martín-Álvarez, P. J.; Victoria Moreno-Arribas, M.; Bartolomé, B. Gut microbial catabolism of grape seed flavan-3-ols by human faecal microbiota. Targetted analysis of precursor compounds, intermediate metabolites and end-products. Food Chem. 2012, 131 (1), 337– 347,  DOI: 10.1016/j.foodchem.2011.08.011
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      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 (2–3), 426– 431,  DOI: 10.1016/j.ijfoodmicro.2011.01.016
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      Comparative study of the inhibitory effects of wine polyphenols on the growth of enological lactic acid bacteria
      Garcia-Ruiz, Almudena; Moreno-Arribas, M. Victoria; Martin-Alvarez, Pedro J.; Bartolome, Begona
      International Journal of Food Microbiology (2011), 145 (2-3), 426-431CODEN: IJFMDD; ISSN:0168-1605. (Elsevier B.V.)
      This paper reports a comparative study of the inhibitory potential of 18 phenolic compds., including hydroxybenzoic acids and their derivs., hydroxycinnamic acids, phenolic alcs. and other related compds., stilbenes, flavan-3-ols and flavonols, on different lactic acid bacteria (LAB) strains of the species Oenococcus oeni, Lactobacillus hilgardii and Pediococcus pentosaceus isolated from wine. In general, flavonols and stilbenes showed the greatest inhibitory effects (lowest IC50 values) on the growth of the strains tested (0.160-0.854 for flavonols and 0.307-0.855 g/L for stilbenes). Hydroxycinnamic acids (IC50 > 0.470 g/L) and hydroxybenzoic acids and esters (IC50 > 1 g/L) exhibited medium inhibitory effect, and phenolic alcs. (IC50 > 2 g/L) and flavanol-3-ols (negligible effect) showed the lowest effect on the growth of the LAB strains studied. In comparison to the antimicrobial additives used in winemaking, IC50 values of most phenolic compds. were higher than those of potassium metabisulphite for O. oeni strains (e.g., around 4-fold higher for quercetin than for potassium metabisulphite), but lower for L. hilgardii and P. pentosaceus strains (e.g., around 2-fold lower for quercetin). Lysozyme IC50 values were negligible for L. hilgardii and P. pentosaceus, and were higher than those corresponding to most of the phenolic compds. tested for O. oeni strains, indicating that lysozyme was less toxic for LAB than the phenolic compds. in wine. SEM confirmed damage of the cell membrane integrity as a consequence of the incubation with antimicrobial agents. These results contribute to the understanding of the inhibitory action of wine phenolics on the progress of malolactic fermn., and also to the development of new alternatives to the use of sulfites in enol.
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      Wang, Y.; Chung, F. F.; Lee, S. M.; Dykes, G. A. Inhibition of attachment of oral bacteria to immortalized human gingival fibroblasts (HGF-1) by tea extracts and tea components. BMC Res. Notes 2013, 6, 143,  DOI: 10.1186/1756-0500-6-143
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      22
      Inhibition of attachment of oral bacteria to immortalized human gingival fibroblasts (HGF-1) by tea extracts and tea components
      Wang Yi; Chung Felicia F L; Lee Sui M; Dykes Gary A
      BMC research notes (2013), 6 (), 143 ISSN:.
      BACKGROUND: Tea has been suggested to promote oral health by inhibiting bacterial attachment to the oral cavity. Most studies have focused on prevention of bacterial attachment to hard surfaces such as enamel. FINDINGS: This study investigated the effect of five commercial tea (green, oolong, black, pu-erh and chrysanthemum) extracts and tea components (epigallocatechin gallate and gallic acid) on the attachment of five oral pathogens (Streptococcus mutans ATCC 25175, Streptococcus mutans ATCC 35668, Streptococcus mitis ATCC 49456, Streptococcus salivarius ATCC 13419 and Actinomyces naeslundii ATCC 51655) to the HGF-1 gingival cell line. Extracts of two of the teas (pu-erh and chrysanthemum) significantly (p < 0.05) reduced attachment of all the Streptococcus strains by up to 4 log CFU/well but effects of other teas and components were small. CONCLUSIONS: Pu-erh and chrysanthemum tea may have the potential to reduce attachment of oral pathogens to gingival tissue and improve the health of oral soft tissues.
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      Muñoz-González, I.; Jiménez-Girón, A.; Martín-Álvarez, P. J.; Bartolomé, B.; Moreno-Arribas, M. V. Profiling of Microbial-Derived Phenolic Metabolites in Human Feces after Moderate Red Wine Intake. J. Agric. Food Chem. 2013, 61 (39), 9470– 9479,  DOI: 10.1021/jf4025135
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      García-Ruiz, A.; Bartolomé, B.; Martínez-Rodríguez, A. J.; Pueyo, E.; Martín-Álvarez, P. J.; Moreno-Arribas, M. V. Potential of phenolic compounds for controlling lactic acid bacteria growth in wine. Food Control 2008, 19 (9), 835– 841,  DOI: 10.1016/j.foodcont.2007.08.018
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      Cueva, C.; Moreno-Arribas, M. V.; Martin-Alvarez, P. J.; Bills, G.; Vicente, M. F.; Basilio, A.; Rivas, C. L.; Requena, T.; Rodriguez, J. M.; Bartolome, B. Antimicrobial activity of phenolic acids against commensal, probiotic and pathogenic bacteria. Res. Microbiol. 2010, 161 (5), 372– 82,  DOI: 10.1016/j.resmic.2010.04.006
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      Antimicrobial activity of phenolic acids against commensal, probiotic and pathogenic bacteria
      Cueva, Carolina; Moreno-Arribas, M. Victoria; Martin-Alvarez, Pedro J.; Bills, Gerald; Vicente, M. Francisca; Basilio, Angela; Rivas, Concepcion Lopez; Requena, Teresa; Rodriguez, Juan M.; Bartolome, Begona
      Research in Microbiology (2010), 161 (5), 372-382CODEN: RMCREW; ISSN:0923-2508. (Elsevier Masson SAS)
      Phenolic acids (benzoic, phenylacetic and phenylpropionic acids) are the most abundant phenolic structures found in fecal water. As an approach towards the exploration of their action in the gut, this paper reports the antimicrobial activity of thirteen phenolic acids towards Escherichia coli, Lactobacillus spp., Staphylococcus aureus, Pseudomonas aeruginosa and Candida albicans. The growth of E. coli ATCC 25922 was inhibited by only four of the phenolic acids tested at a concn. of 1000 μg/mL, whereas pathogenic E. coli O157:H7 (CECT 5947) was susceptible to ten of them. The genetically manipulated E. coli lpxC/tolC strain was highly susceptible to phenolic acids. The growth of lactobacilli (Lactobacillus paraplantarum LCH7, Lactobacillus plantarum LCH17, Lactobacillus fermentum LPH1, L. fermentum CECT 5716, Lactobacillus brevis LCH23, and Lactobacillus coryniformis CECT 5711) and pathogens (S. aureus EP167 and C. albicans MY1055) was also inhibited by phenolic acids, but to varying extents. Only P. aeruginosa PAO1 was not susceptible to any of the phenolic compds. tested. Structure-activity relationships of phenolic acids and some of their diet precursors [(+)-catechin and (-)-epicatechin] were established, based on multivariate anal. of microbial activities. The antimicrobial properties of phenolic acids reported in this paper might be relevant in vivo.
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    26. 26
      Cueva, C.; Mingo, S.; Munoz-Gonzalez, I.; Bustos, I.; Requena, T.; del Campo, R.; Martin-Alvarez, P. J.; Bartolome, B.; Moreno-Arribas, M. V. Antibacterial activity of wine phenolic compounds and oenological extracts against potential respiratory pathogens. Lett. Appl. Microbiol. 2012, 54 (6), 557– 63,  DOI: 10.1111/j.1472-765X.2012.03248.x
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      26
      Antibacterial activity of wine phenolic compounds and oenological extracts against potential respiratory pathogens
      Cueva, C.; Mingo, S.; Munoz-Gonzalez, I.; Bustos, I.; Requena, T.; del Campo, R.; Martin-Alvarez, P. J.; Bartolome, B.; Moreno-Arribas, M. V.
      Letters in Applied Microbiology (2012), 54 (6), 557-563CODEN: LAMIE7; ISSN:0266-8254. (Wiley-Blackwell)
      The aim was to investigate the effect of seven wine phenolic compds. and six oenol. phenolic exts. on the growth of pathogenic bacteria assocd. with respiratory diseases (Pseudomonas aeruginosa, Staphylococcus aureus, Moraxella catarrhalis, Enterococcus faecalis, Streptococcus sp Group F, Streptococcus agalactiae and Streptococcus pneumoniae). Antimicrobial activity was detd. using a microdilution method and quantified as IC50. Mor. catarrhalis was the most susceptible specie to phenolic compds. and exts. Gallic acid and Et gallate were the compds. that showed the greatest antimicrobial activity. Regarding phenolic exts., GSE (grape seed ext.) and GSE-O (oligomeric-rich fraction from GSE) were the ones that displayed the strongest antimicrobial effects. Results highlight the antimicrobial properties of wine phenolic compds. and oenol. exts. against potential respiratory pathogens. The antimicrobial activity of wine phenolic compds. was influenced by the type of phenolic compds. Gram-neg. bacteria were more susceptible than Gram-pos. bacteria to the action of phenolic compds. and exts.; however, the effect was species-dependent. The ability to inhibit the growth of respiratory pathogenic bacteria as shown by several wine phenolic compds. and oenol. exts. warrants further investigations to explore the use of grape and wine prepns. in oral hygiene.
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    27. 27
      Almeida, A. A. P.; Naghetini, C. C.; Santos, V. R.; Antonio, A. G.; Farah, A.; Glória, M. B. A. Influence of natural coffee compounds, coffee extracts and increased levels of caffeine on the inhibition of Streptococcus mutans. Food Res. Int. 2012, 49 (1), 459– 461,  DOI: 10.1016/j.foodres.2012.07.026
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      27
      Influence of natural coffee compounds, coffee extracts and increased levels of caffeine on the inhibition of Streptococcus mutans
      Almeida, A. A. P.; Naghetini, C. C.; Santos, V. R.; Antonio, A. G.; Farah, A.; Gloria, M. B. A.
      Food Research International (2012), 49 (1), 459-461CODEN: FORIEU; ISSN:0963-9969. (Elsevier B.V.)
      The inhibition of Streptococcus mutans by Coffea arabica exts. incorporated or not with natural coffee compds. was investigated by the disk diffusion method. Addnl., the turbidimetric test was used to verify the influence of caffeine concn. on the inhibition of S. mutans. Exts. of different samples of Arabica coffee showed antibacterial activity against S. mutans. The inhibitory effect was not affected by the brewing method (filtered or espresso) or by the different Arabica coffee samples. Plain caffeine, trigonelline, caffeic acid, protocatechuic acid and chlorogenic acid at 2.0 mg/mL provided similar antimicrobial effect against S. mutans. However, there was an increase in the antibacterial activity when these compds. were added to the coffee ext., except for chlorogenic acid which did not affect the inhibitory effect. Caffeine at concns. found in Arabica beverages inhibited S. mutans temporarily, whereas higher caffeine concns. provided a stronger and longer lasting inhibition.
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      Barrientos, L.; Herrera, C. L.; Montenegro, G.; Ortega, X.; Veloz, J.; Alvear, M.; Cuevas, A.; Saavedra, N.; Salazar, L. A. Chemical and botanical characterization of Chilean propolis and biological activity on cariogenic bacteria Streptococcus mutans and Streptococcus sobrinus. Braz. J. Microbiol. 2013, 44 (2), 577– 85,  DOI: 10.1590/S1517-83822013000200038
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      28
      Chemical and botanical characterization of Chilean propolis and biological activity on cariogenic bacteria Streptococcus mutans and Streptococcus sobrinus
      Barrientos, Leticia; Herrera, Christian L.; Montenegro, Gloria; Ortega, Ximena; Veloz, Jorge; Alvear, Marysol; Cuevas, Alejandro; Saavedra, Nicolas; Salazar, Luis A.
      Brazilian Journal of Microbiology (2013), 44 (2), 577-585, 9 pp.CODEN: BJMRAH; ISSN:1517-8382. (Brazilian Society of Microbiology)
      Propolis is a non-toxic natural substance with multiple pharmacol. properties including anticancer, antioxidant, fungicidal, antibacterial, antiviral and anti-inflammatory among others. The aim of this study was to det. the chem. and botanical characterization of Chilean propolis samples and to evaluate their biol. activity against the cariogenic bacteria Streptococcus mutans and Streptococcus sobrinus. Twenty propolis samples were obtained from beekeeping producers from the central and southern regions of Chile. The botanical profile was detd. by palynol. anal. Total phenolic contents were detd. using colorimetric assays. Reverse phase HPLC and HPLC-MS were used to det. the chem. compn. The min. inhibitory concn. (MIC) was detd. on S. mutans and S. sobrinus. All propolis samples were dominated by structures from native plant species. The characterization by HPLC/MS, evidenced the presence of quercetin, myricetin, kaempferol, rutine, pinocembrin, coumaric acid, caffeic acid and caffeic acid phenethyl ester, that have already been described in these propolis with conventional HPLC. Although all propolis samples inhibited the mutans streptococci growth, it was obsd. a wide spectrum of action (MIC 0.90 to 8.22 μg mL-1). Given that results it becomes increasingly evident the need of standardization procedures, where we combine both the detn. of botanical and the chem. characterization of the exts. Research conducted to date, describes a promising effectiveness of propolis in the prevention of caries and other diseases of the oral cavity, making it necessary to develop studies to identify and understand the therapeutic targets or mechanisms of mol. action of the various compds. present on them.
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    29. 29
      Lima, V. N.; Oliveira-Tintino, C. D. M.; Santos, E. S.; Morais, L. P.; Tintino, S. R.; Freitas, T. S.; Geraldo, Y. S.; Pereira, R. L. S.; Cruz, R. P.; Menezes, I. R. A.; Coutinho, H. D. M. Antimicrobial and enhancement of the antibiotic activity by phenolic compounds: Gallic acid, caffeic acid and pyrogallol. Microb. Pathog. 2016, 99, 56– 61,  DOI: 10.1016/j.micpath.2016.08.004
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      29
      Antimicrobial and enhancement of the antibiotic activity by phenolic compounds: Gallic acid, caffeic acid and pyrogallol
      Lima, Valeria N.; Oliveira-Tintino, Cicera D. M.; Santos, Enaide S.; Morais, Luis P.; Tintino, Saulo R.; Freitas, Thiago S.; Geraldo, Yuri S.; Pereira, Raimundo L. S.; Cruz, Rafael P.; Menezes, Irwin R. A.; Coutinho, Henrique D. M.
      Microbial Pathogenesis (2016), 99 (), 56-61CODEN: MIPAEV; ISSN:0882-4010. (Elsevier Ltd.)
      The indiscriminate use of antimicrobial drugs has increased the spectrum of exposure of these organisms. In our studies, these phenolic compds. were evaluated: gallic acid, caffeic acid and pyrogallol. The antibacterial, antifungal and modulatory of antibiotic activities of these compds. were assayed using microdilution method of Min. Inhibitory Concn. (MIC) to bacteria and Min. Fungicide Concn. (MFC) to fungi. The modulation was made by comparisons of the MIC and MFC of the compds. alone and combined with drugs against bacteria and fungi resp., using a sub-inhibitory concn. of 128 μg/mL of substances (MIC/8). All substances not demonstrated clin. relevant antibacterial activity with a MIC above ≥1024 μg/mL. As a result, we obsd. that the caffeic acid presented a potentiating antibacterial effect over the 3 groups of bacteria studied. Pyrogallol showed a synergistic effect with two of the antibiotics tested, but only against Staphylococcus aureus. In general, caffeic acid was the substance that presented with the greatest no. of antibiotics and with the greatest no. of bacteria. In relation to the antifungal activity of all the compds., the verified results were ≥1024 μg/mL, not demonstrating significant activity. Regarding potentiation of the effect of fluconazole, was obsd. synergistic effect only when assayed against Candida tropicalis, with all substances. Therefore, as can be seen, the compds. presented as substances that can be promising potentiating agents of antimicrobial drugs, even though they do not have direct antibacterial and antifungal action.
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    30. 30
      Nakamura, K.; Ishiyama, K.; Sheng, H.; Ikai, H.; Kanno, T.; Niwano, Y. Bactericidal Activity and Mechanism of Photoirradiated Polyphenols against Gram-Positive and -Negative Bacteria. J. Agric. Food Chem. 2015, 63 (35), 7707– 13,  DOI: 10.1021/jf5058588
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      Bactericidal activity and mechanism of photoirradiated polyphenols against Gram-positive and -negative bacteria
      Nakamura, Keisuke; Ishiyama, Kirika; Sheng, Hong; Ikai, Hiroyo; Kanno, Taro; Niwano, Yoshimi
      Journal of Agricultural and Food Chemistry (2015), 63 (35), 7707-7713CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
      The bactericidal effect of various types of photoirradiated polyphenols against Gram-pos. and -neg. bacteria was evaluated in relation to the mode of action. Gram-pos. bacteria (Enterococcus faecalis, Staphylococcus aureus, and Streptococcus mutans) and Gram-neg. bacteria (Aggregatibacter actinomycetemcomitans, Escherichia coli, and Pseudomonas aeruginosa) suspended in a 1 mg/mL polyphenol aq. soln. (caffeic acid, gallic acid, chlorogenic acid, epigallocatechin, epigallocatechin gallate, and proanthocyanidin) were exposed to LED light (wavelength, 400 nm; irradiance, 260 mW/cm2) for 5 or 10 min. Caffeic acid and chlorogenic acid exerted the highest bactericidal activity followed by gallic acid and proanthocyanidin against both Gram-pos. and -neg. bacteria. It was also demonstrated that the disinfection treatment induced oxidative damage of bacterial DNA, which suggests that polyphenols are incorporated into bacterial cells. The present study suggests that blue light irradn. of polyphenols could be a novel disinfection treatment.
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      Furiga, A.; Lonvaud-Funel, A.; Badet, C. In vitro study of antioxidant capacity and antibacterial activity on oral anaerobes of a grape seed extract. Food Chem. 2009, 113 (4), 1037– 1040,  DOI: 10.1016/j.foodchem.2008.08.059
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      Ben Lagha, A.; Dudonne, S.; Desjardins, Y.; Grenier, D. Wild Blueberry (Vaccinium angustifolium Ait.) Polyphenols Target Fusobacterium nucleatum and the Host Inflammatory Response: Potential Innovative Molecules for Treating Periodontal Diseases. J. Agric. Food Chem. 2015, 63 (31), 6999– 7008,  DOI: 10.1021/acs.jafc.5b01525
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      Daglia, M.; Papetti, A.; Grisoli, P.; Aceti, C.; Dacarro, C.; Gazzani, G. Antibacterial Activity of Red and White Wine against Oral Streptococci. J. Agric. Food Chem. 2007, 55 (13), 5038– 5042,  DOI: 10.1021/jf070352q
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      Krachler, A. M.; Orth, K. Targeting the bacteria–host interface: Strategies in anti-adhesion therapy. Virulence 2013, 4 (4), 284– 294,  DOI: 10.4161/viru.24606
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      Yamanaka, A.; Kimizuka, R.; Kato, T.; Okuda, K. Inhibitory effects of cranberry juice on attachment of oral streptococci and biofilm formation. Oral Microbiol. Immunol. 2004, 19 (3), 150– 4,  DOI: 10.1111/j.0902-0055.2004.00130.x
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      Inhibitory effects of cranberry juice on attachment of oral streptococci and biofilm formation
      Yamanaka A; Kimizuka R; Kato T; Okuda K
      Oral microbiology and immunology (2004), 19 (3), 150-4 ISSN:0902-0055.
      Cranberry juice is known to inhibit bacterial adhesion. We examined the inhibitory effect of cranberry juice on the adhesion of oral streptococci strains labeled with [3H]-thymidine to saliva-coated hydroxyapatite beads (s-HA). When the bacterial cells were momentarily exposed to cranberry juice, their adherence to s-HA decreased significantly compared with the control (P < 0.01). Their hydrophobicity also decreased dependently with the concentration of cranberry juice. We also evaluated the inhibitory effect of cranberry juice on biofilm formation. By using a microplate system, we found that the high molecular mass constituents of cranberry juice inhibited the biofilm formation of the tested streptococci. The inhibitory activity was related to the reduction of the hydrophobicity. The present findings suggest that cranberry juice component(s) can inhibit colonization by oral streptococci to the tooth surface and can thus slow development of dental plaque.
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      Berlutti, F.; Catizone, A.; Ricci, G.; Frioni, A.; Natalizi, T.; Valenti, P.; Polimeni, A. Streptococcus mutans and Streptococcus sobrinus are able to adhere and invade human gingival fibroblast cell line. Int. J. Immunopathol. Pharmacol. 2010, 23 (4), 1253– 60,  DOI: 10.1177/039463201002300430
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      Streptococcus mutans and Streptococcus sobrinus are able to adhere and invade human gingival fibroblast cell line
      Berlutti F; Catizone A; Ricci G; Frioni A; Natalizi T; Valenti P; Polimeni A
      International journal of immunopathology and pharmacology (2010), 23 (4), 1253-60 ISSN:0394-6320.
      Streptococcus mutans and Streptococcus sobrinus, the principal etiologic agents of caries decay of teeth, are generally acquired in oral cavity at the moment of tooth eruption. However, as S. mutans has been detected in oral cavity of predentate children, the eruption of teeth seems not to be a necessary prerequisite, suggesting that this species may be not confined to dental plaque. Here, we evaluate the ability of S. mutans and S. sobrinus in planktonic and biofilm lifestyle to adhere, invade and survive within human gingival fibroblast (HGF-1) cells. Planktonic and biofilm streptococci adhered and invaded host cells to different extents, showing higher efficiencies of biofilm than planktonic counterparts. Moreover, planktonic and biofilm streptococci showed the same percentage of survival within host cells. Transmission electron and confocal microscopy observations confirmed intracellular localization of planktonic and biofilm bacteria. The adhesion, invasion and survival abilities within human oral cells may be considered S. mutans and S. sobrinus virulence mechanisms to colonize and persist in the oral cavity in the absence of tooth surface.
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      Daglia, M.; Stauder, M.; Papetti, A.; Signoretto, C.; Giusto, G.; Canepari, P.; Pruzzo, C.; Gazzani, G. Isolation of red wine components with anti-adhesion and anti-biofilm activity against Streptococcus mutans. Food Chem. 2010, 119 (3), 1182– 1188,  DOI: 10.1016/j.foodchem.2009.08.037
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      Ben Lagha, A.; Haas, B.; Grenier, D. Sci. Rep. 2017, 7, 44815,  DOI: 10.1038/srep44815
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      Tea polyphenols inhibit the growth and virulence properties of Fusobacterium nucleatum
      Ben Lagha, Amel; Haas, Bruno; Grenier, Daniel
      Scientific Reports (2017), 7 (), 44815CODEN: SRCEC3; ISSN:2045-2322. (Nature Publishing Group)
      Fusobacterium nucleatum plays a key role in creating the pathogenic subgingival biofilm that initiates destructive periodontitis. It is also a common resident of the human gastrointestinal tract and has been assocd. with inflammatory bowel disease. The aim of the present study was to investigate the effects of green and black tea exts. as well as two of their bioactive components, EGCG and theaflavins, on the growth and virulence properties of F. nucleatum. The tea exts. and components displayed various degrees of antibacterial activity that may involve damage to the bacterial cell membrane and the chelation of iron. They also prevented biofilm formation by F. nucleatum at concns. that did not interfere with bacterial growth. In addn., the treatment of a pre-formed F. nucleatum biofilm with the green tea ext. and EGCG caused a time-dependent decrease in biofilm viability. The green and black tea exts., EGCG, and theaflavins decreased the adherence of F. nucleatum to oral epithelial cells and matrix proteins. Moreover, these tea components also attenuated F. nucleatum-mediated hemolysis and hydrogen sulfide prodn., two other virulence factors expressed by this bacterium. In summary, this study showed that tea polyphenols may be of interest for treating F. nucleatum-assocd. disorders.
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      Saito, Y.; Fujii, R.; Nakagawa, K. I.; Kuramitsu, H. K.; Okuda, K.; Ishihara, K. Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis. Oral Microbiol. Immunol. 2008, 23 (1), 1– 6,  DOI: 10.1111/j.1399-302X.2007.00380.x
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      Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis
      Saito Y; Fujii R; Nakagawa K-I; Kuramitsu H K; Okuda K; Ishihara K
      Oral microbiology and immunology (2008), 23 (1), 1-6 ISSN:0902-0055.
      BACKGROUND/AIMS: Bacterial infection is a major cause of periapical periodontitis. Eradication of these microorganisms from apical lesions is essential to the success of endodontic treatment. The aim of this study was to clarify the molecular interaction between Fusobacterium nucleatum, Porphyromonas gingivalis and other microorganisms associated with periapical periodontitis. METHODS: Microorganisms isolated from periapical lesions were inoculated into type-I collagen-coated polystyrene microtiter plates and maintained at 37 degrees C under anaerobic conditions for 2 days, after which, the quantity of organized biofilm on the plates was evaluated by crystal violet staining. Growth enhancement via soluble factor was evaluated by separated coculture using a 0.4-mum membrane filter. RESULTS: F. nucleatum exhibited strong adherence to type-I collagen-coated polystyrene microplates. Biofilm formation by F. nucleatum was significantly enhanced by P. gingivalis. It was complemented by compartmentalized coculture with P. gingivalis. Enhancement of biofilm formation by P. gingivalis was only slightly reduced by inactivation of its autoinducer-2-producing gene luxS. CONCLUSION: The results suggest that P. gingivalis enhances biofilm formation by F. nucleatum by releasing diffusible signaling molecules other than autoinducer-2.
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      Diaz, P. I.; Zilm, P. S.; Rogers, A. H. Fusobacterium nucleatum supports the growth of Porphyromonas gingivalis in oxygenated and carbon-dioxide-depleted environments. Microbiology (London, U. K.) 2002, 148 (2), 467– 472,  DOI: 10.1099/00221287-148-2-467
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      Kolenbrander, P. E.; Palmer, R. J., Jr; Periasamy, S.; Jakubovics, N. S. Oral multispecies biofilm development and the key role of cell–cell distance. Nat. Rev. Microbiol. 2010, 8, 471,  DOI: 10.1038/nrmicro2381
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      Oral multispecies biofilm development and the key role of cell-cell distance
      Kolenbrander, Paul E.; Palmer, Robert J.; Periasamy, Saravanan; Jakubovics, Nicholas S.
      Nature Reviews Microbiology (2010), 8 (7), 471-480CODEN: NRMACK; ISSN:1740-1526. (Nature Publishing Group)
      Growth of oral bacteria in situ requires adhesion to a surface because the const. flow of host secretions thwarts the ability of planktonic cells to grow before they are swallowed. Therefore, oral bacteria evolved to form biofilms on hard tooth surfaces and on soft epithelial tissues, which often contain multiple bacterial species. Because these biofilms are easy to study, they have become the paradigm of multispecies biofilms. In this Review we describe the factors involved in the formation of these biofilms, including the initial adherence to the oral tissues and teeth, cooperation between bacterial species in the biofilm, signalling between the bacteria and its role in pathogenesis, and the transfer of DNA between bacteria. In all these aspects distance between cells of different species is integral for oral biofilm growth.
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      Mira, A. Oral microbiome studies: potential diagnostic and therapeutic implications. Adv. Dent. Res. 2018, 29, 71– 77,  DOI: 10.1177/0022034517737024
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      Oral Microbiome Studies: Potential Diagnostic and Therapeutic Implications
      Mira A
      Advances in dental research (2018), 29 (1), 71-77 ISSN:.
      Understanding the microbiology of dental caries is not a mere academic exercise; it provides the basis for preventive, diagnostic, and treatment strategies and gives the dentist a theoretical framework to become a better professional. The last years have seen the development of new research methodologies, ranging from high-throughput sequencing or "omics" techniques to new fluorescence microscopy applications and microfluidics, which have allowed the study of the oral microbiome to an unprecedented level of detail. Those studies have provided new insights about oral biofilm formation, biomarkers of caries risk, microbial etiology, appropriate sampling, identification of health-associated bacteria, and new anticaries strategies, among others. Several pitfalls are associated with the new technologies, including a small number of samples per study group, elevated cost, and genus- or species-based analyses that do not take into consideration intraspecies variability. However, the new data strongly suggest that saliva may not be an appropriate sample for etiological studies or for bacterial caries-risk tests, that microbial composition alone may be insufficient to predict caries risk, and that antimicrobial or immunization strategies targeting single species are unlikely to be effective. Strategies directed toward modulation of the oral biofilm, such as pre- and probiotics, emerge as promising new approaches to prevent tooth decay.
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      Labrecque, J.; Bodet, C.; Chandad, F.; Grenier, D. Effects of a high-molecular-weight cranberry fraction on growth, biofilm formation and adherence of Porphyromonas gingivalis. J. Antimicrob. Chemother. 2006, 58 (2), 439– 443,  DOI: 10.1093/jac/dkl220
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      Effects of a high-molecular-weight cranberry fraction on growth, biofilm formation and adherence of Porphyromonas gingivalis
      Labrecque, Julie; Bodet, Charles; Chandad, Fatiha; Grenier, Daniel
      Journal of Antimicrobial Chemotherapy (2006), 58 (2), 439-443CODEN: JACHDX; ISSN:0305-7453. (Oxford University Press)
      Porphyromonas gingivalis is a major etiol. agent of periodontitis, a destructive disease affecting the tooth-supporting tissues. Recent reports have indicated that high-mol.-wt. mols. from cranberry juice conc. can prevent the attachment of human pathogens to host tissues. The aim of the present study was to investigate the effect of non-dialysable material (NDM) prepd. from cranberry juice conc. on growth, biofilm formation and adherence properties of P. gingivalis. The effect of cranberry NDM on biofilm formation was studied using a polystyrene microplate assay and by SEM. The effect of cranberry NDM on the attachment properties of P. gingivalis was evaluated by a microplate assay in which mammalian proteins were immobilized into wells. Our results indicated that cranberry NDM is a potent inhibitor of biofilm formation by P. gingivalis. However, it has no effect on growth and viability of bacteria. Cranberry NDM also prevented significantly the attachment of P. gingivalis to surfaces coated with type I collagen, fibrinogen or human serum. Our data suggest that cranberry constituents may have a beneficial effect for the prevention and treatment of periodontitis by reducing the capacity of P. gingivalis to colonize periodontal sites.
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      https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD28Xotl2lsLs%253D&md5=c388ead7455f1cef238747ec30529587
    44. 44
      La, V. D.; Howell, A. B.; Grenier, D. Anti-Porphyromonas gingivalis and anti-inflammatory activities of A-type cranberry proanthocyanidins. Antimicrob. Agents Chemother. 2010, 54 (5), 1778– 84,  DOI: 10.1128/AAC.01432-09
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      Silva, A. P.; Goncalves, R. S.; Borges, A. F.; Bedran-Russo, A. K.; Shinohara, M. S. Effectiveness of plant-derived proanthocyanidins on demineralization on enamel and dentin under artificial cariogenic challenge. Journal of applied oral science: revista FOB 2015, 23 (3), 302– 9,  DOI: 10.1590/1678-775720140304
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      Effectiveness of plant-derived proanthocyanidins on demineralization on enamel and dentin under artificial cariogenic challenge
      Silva Ana Paula Pereira da; Shinohara Mirela Sanae; Goncalves Rafael Simoes; Borges Ana Flavia Sanches; Bedran-Russo Ana Karina
      Journal of applied oral science : revista FOB (2015), 23 (3), 302-9 ISSN:.
      UNLABELLED: Dental caries is considered a disease of high prevalence and a constant problem in public health. Proanthocyanidins (PAs) are substances that have been the target of recent studies aiming to control or treat caries. OBJECTIVE: The aim of this in vitro study was to evaluate the efficacy of a treatment with grape seed extract, under cariogenic challenge, to minimize or even prevent the onset of caries in the enamel and dentin. MATERIAL AND METHODS: Blocks of enamel and dentin (6.0x6.0 mm) were obtained from bovine central incisors, polished, and selected by analysis of surface microhardness (SH). The blocks were randomly divided into 3 groups (n=15), according to the following treatments: GC (control), GSE (grape seed extract), GF (fluoride - 1,000 ppm). The blocks were subjected to 6 daily pH cycles for 8 days. Within the daily cycling, the specimens were stored in buffered solution. The blocks were then analyzed for perpendicular and surface hardness and polarized light microscopy. RESULTS: The means were subjected to statistical analysis using the ANOVA and Fisher's PLSD tests (p<0.05). For enamel SH, GF showed the highest hardness values. In the dentin, GF was also the one that showed higher hardness values, followed by GSE. Regarding the cross-sectional hardness values, all groups behaved similarly in both the enamel and dentin. The samples that were treated with GSE and fluoride (GF) showed statistically higher values than the control. CONCLUSION: Based on the data obtained in this in vitro study, it is suggested that grape seed extract inhibits demineralization of artificial carious lesions in both the enamel and dentin, but in a different scale in each structure and in a smaller scale when compared to fluoride.
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    46. 46
      Park, H.-J.; Jeong, S.-K.; Kim, S.-R.; Bae, S.-K.; Kim, W.-S.; Jin, S.-D.; Koo, T. H.; Jang, H.-O.; Yun, I.; Kim, K.-W.; Bae, M.-K. Resveratrol inhibits Porphyromonas gingivalis lipopolysaccharide-induced endothelial adhesion molecule expression by suppressing NF-κB activation. Arch. Pharmacal Res. 2009, 32 (4), 583– 591,  DOI: 10.1007/s12272-009-1415-7
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      Resveratrol inhibits Porphyromonas gingivalis lipopolysaccharide-induced endothelial adhesion molecule expression by suppressing NF-κB activation
      Park, Hyun-Joo; Jeong, Seong-Kyoon; Kim, Su-Ryun; Bae, Soo-Kyung; Kim, Woo-Sik; Jin, Seong-Deok; Koo, Tae Hyeon; Jang, Hye-Ock; Yun, Il; Kim, Kyu-Won; Bae, Moon-Kyoung
      Archives of Pharmacal Research (2009), 32 (4), 583-591CODEN: APHRDQ; ISSN:0253-6269. (Pharmaceutical Society of Korea)
      P. gingivalis is a major pathogen that is involved in the onset and progression of periodontal disease. This study investigated the effect of resveratrol, a naturally occurring polyphenol, on P. gingivalis LPS-accelerated vascular inflammation, a key step in the progression of periodontitis. Resveratrol significantly inhibited the P. gingivalis LPS-induced adhesion of leukocytes to endothelial cells and to the aortic endothelium by down-regulating the cell adhesion mols., ICAM-1 and VCAM-1. Moreover, the inhibition of the P. gingivalis LPS-induced cell adhesion mols. by resveratrol was mainly mediated by nuclear factor-κB (NF-κB). Resveratrol suppressed P. gingivalis LPS-stimulated IκBα phosphorylation and nuclear translocation of the p65 subunit of NF-κB in HMECs. Overall, these findings suggest that resveratrol significantly attenuates the P. gingivalis LPS-induced monocyte adhesion to the endothelium by suppressing the expression of the NF-κB-dependent cell adhesion mols., suggesting its therapeutic role in periodontal pathogen-induced vascular inflammation.
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      Minagawa, T.; Okui, T.; Takahashi, N.; Nakajima, T.; Tabeta, K.; Murakami, S.; Yamazaki, K. Resveratrol suppresses the inflammatory responses of human gingival epithelial cells in a SIRT1 independent manner. J. Periodontal Res. 2015, 50 (5), 586– 593,  DOI: 10.1111/jre.12238
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      Resveratrol suppresses the inflammatory responses of human gingival epithelial cells in a SIRT1 independent manner
      Minagawa, T.; Okui, T.; Takahashi, N.; Nakajima, T.; Tabeta, K.; Murakami, S.; Yamazaki, K.
      Journal of Periodontal Research (2015), 50 (5), 586-593CODEN: JPDRAY; ISSN:0022-3484. (Wiley-Blackwell)
      Background and Objective : In periodontitis, chronic infection by periodontopathic bacteria induces uncontrolled inflammation, which leads to periodontal tissue destruction. Human gingival epithelial cells (HGECs) constitute a crit. first line of defense against periodontopathic bacteria, both as a phys. barrier and as regulators of inflammation. Resveratrol, a polyphenol found in grapes and red wine, reportedly has anti-inflammatory properties. Therefore, we investigated the effects of resveratrol on the Porphyromonas gingivalis-induced inflammatory responses of HGECs and their mechanism. Material and Methods : We stimulated the HGEC line, epi 4, with live or heat-killed P. gingivalis in the presence of resveratrol, and analyzed expressions of the interleukin-8, monocyte chemoattractant protein-1 and interleukin-1β genes. We detd. the involvement of SIRT1 in the effect of resveratrol using sirtinol (a SIRT1 inhibitor) or SIRT1 knockdown. We also examd. whether the effects were mediated by activation of AMP-activated kinase, suppression of reactive oxygen species, or inhibition of nuclear factor-κB (NF-κB). Results : Resveratrol treatment decreased the expression of inflammatory cytokines and slightly increased the expression of SIRT1. However, neither SIRT1 inhibition nor SIRT1 knockdown counteracted its anti-inflammatory effects. Although resveratrol did not affect AMP-activated kinase activation or reactive oxygen species prodn., it slightly suppressed NF-κB translocation when cells were stimulated with heat-killed P. gingivalis. Conclusion : Resveratrol suppressed the inflammatory responses of P. gingivalis-stimulated HGECs, probably by inhibiting NF-κB signaling but independent of SIRT1.
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      Sakanaka, S.; Aizawa, M.; Kim, M.; Yamamoto, T. Inhibitory Effects of Green Tea Polyphenols on Growth and Cellular Adherence of an Oral Bacterium, Porphyromonas gingivalis. Biosci., Biotechnol., Biochem. 1996, 60 (5), 745– 749,  DOI: 10.1271/bbb.60.745
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      Kline, K. A.; Fälker, S.; Dahlberg, S.; Normark, S.; Henriques-Normark, B. Bacterial Adhesins in Host-Microbe Interactions. Cell Host Microbe 2009, 5 (6), 580– 592,  DOI: 10.1016/j.chom.2009.05.011
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      Bacterial adhesins in host-microbe interactions
      Kline, Kimberly A.; Faelker, Stefan; Dahlberg, Sofia; Normark, Staffan; Henriques-Normark, Birgitta
      Cell Host & Microbe (2009), 5 (6), 580-592CODEN: CHMECB; ISSN:1931-3128. (Cell Press)
      A review. Most commensal and pathogenic bacteria interacting with eukaryotic hosts express adhesive mols. on their surfaces that promote interaction with host cell receptors or with sol. macromols. Even though bacterial attachment to epithelial cells may be beneficial for bacterial colonization, adhesion may come at a cost because bacterial attachment to immune cells can facilitate phagocytosis and clearing. Many pathogenic bacteria have solved this dilemma by producing an antiphagocytic surface layer usually consisting of polysaccharide and by expressing their adhesins on polymeric structures that extend out from the cell surface. In this review, we will focus on the interaction between bacterial adhesins and the host, with an emphasis on pilus-like structures.
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      González de Llano, D.; Gil-Sánchez, I.; Esteban-Fernández, A.; Ramos, A. M.; Fernández-Díaz, M.; Cueva, C.; Moreno-Arribas, M. V.; Bartolomé, B. Reciprocal beneficial effects between wine polyphenols and probiotics: an exploratory study. Eur. Food Res. Technol. 2017, 243 (3), 531– 538,  DOI: 10.1007/s00217-016-2770-5
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      Garcia-Ruiz, A.; Gonzalez de Llano, D.; Esteban-Fernandez, A.; Requena, T.; Bartolome, B.; Moreno-Arribas, M. V. Assessment of probiotic properties in lactic acid bacteria isolated from wine. Food Microbiol. 2014, 44, 220– 5,  DOI: 10.1016/j.fm.2014.06.015
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      Assessment of probiotic properties in lactic acid bacteria isolated from wine
      Garcia-Ruiz, Almudena; Gonzalez de Llano, Dolores; Esteban-Fernandez, Adelaida; Requena, Teresa; Bartolome, Begona; Moreno-Arribas, M. Victoria
      Food Microbiology (2014), 44 (), 220-225CODEN: FOMIE5; ISSN:0740-0020. (Elsevier Ltd.)
      Probiotic properties are highly strain-dependent but rarely studied in enol. lactic acid bacteria (LAB). In this study, the probiotic features of 11 strains of Lactobacillus spp., Pediococcus spp., and Oenococcus oeni, including saliva and acid resistance, bile tolerance and exopolysaccharides' prodn., were investigated. The assays included two probiotic ref. strains (Lactobacillus plantarum CLC 17 and Lactobacillus fermentum CECT5716). The Lactobacillus and Pediococcus strains showed high resistance to lysozyme (>80% resistance to 100 mg/L of lysozyme under conditions simulating the in vivo diln. by saliva) and were capable of surviving at low pH values (pH 1.8) and bile salts, suggesting good adaptation of the wine strains to gastrointestinal conditions. The ability of the strains to adhere to the intestinal mucosa and the inhibition of the adhesion of Escherichia coli to human intestinal cells were also evaluated. Adhesion levels of enol. LAB to Caco-2 cells varied from 0.37% to 12.2%, depending on the strain. In particular, Pediococcus pentosaceus CIAL-86 showed a high percentage of adhesion to intestinal cells (>12%), even higher than that shown by the probiotic ref. strains, and a high anti-adhesion activity against E. coli CIAL-153 (>30%), all of which support this wine LAB strain as a potential probiotic.
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    52. 52
      Pereira-Caro, G.; Oliver, C. M.; Weerakkody, R.; Singh, T.; Conlon, M.; Borges, G.; Sanguansri, L.; Lockett, T.; Roberts, S. A.; Crozier, A.; Augustin, M. A. Chronic administration of a microencapsulated probiotic enhances the bioavailability of orange juice flavanones in humans. Free Radical Biol. Med. 2015, 84, 206– 14,  DOI: 10.1016/j.freeradbiomed.2015.03.010
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      Chronic administration of a microencapsulated probiotic enhances the bioavailability of orange juice flavanones in humans
      Pereira-Caro, Gema; Oliver, Christine M.; Weerakkody, Rangika; Singh, Tanoj; Conlon, Michael; Borges, Gina; Sanguansri, Luz; Lockett, Trevor; Roberts, Susan A.; Crozier, Alan; Augustin, Mary Ann
      Free Radical Biology & Medicine (2015), 84 (), 206-214CODEN: FRBMEH; ISSN:0891-5849. (Elsevier B.V.)
      Orange juice (OJ) flavanones are bioactive polyphenols that are absorbed principally in the large intestine. Ingestion of probiotics has been assocd. with favorable changes in the colonic microflora. The present study examd. the acute and chronic effects of orally administered Bifidobacterium longum R0175 on the colonic microflora and bioavailability of OJ flavanones in healthy volunteers. In an acute study volunteers drank OJ with and without the microencapsulated probiotic, whereas the chronic effects were examd. when OJ was consumed after daily supplementation with the probiotic over 4 wk. Bioavailability, assessed by 0-24 h urinary excretion, was similar when OJ was consumed with and without acute probiotic intake. Hesperetin-O-glucuronides, naringenin-O-glucuronides, and hesperetin-3'-O-sulfate were the main urinary flavanone metabolites. The overall urinary excretion of these metabolites after OJ ingestion and acute probiotic intake corresponded to 22% of intake, whereas excretion of key colon-derived phenolic and arom. acids was equiv. to 21% of the ingested OJ (poly)phenols. Acute OJ consumption after chronic probiotic intake over 4 wk resulted in the excretion of 27% of flavanone intake, and excretion of selected phenolic acids also increased significantly to 43% of (poly)phenol intake, corresponding to an overall bioavailability of 70%. Neither the probiotic bacterial profiles of stools nor the stool moisture, wt., pH, or levels of short-chain fatty acids and phenols differed significantly between treatments. These findings highlight the pos. effect of chronic, but not acute, intake of microencapsulated B. longum R0175 on the bioavailability of OJ flavanones.
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      Faria, A.; Fernandes, I.; Norberto, S.; Mateus, N.; Calhau, C. Interplay between anthocyanins and gut microbiota. J. Agric. Food Chem. 2014, 62 (29), 6898– 902,  DOI: 10.1021/jf501808a
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      Interplay between Anthocyanins and Gut Microbiota
      Faria, Ana; Fernandes, Iva; Norberto, Sonia; Mateus, Nuno; Calhau, Conceicao
      Journal of Agricultural and Food Chemistry (2014), 62 (29), 6898-6902CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
      A review. Anthocyanins are naturally occurring compds. abundant in the human diet. Evidence has accumulated regarding the pos. assocn. of their intake with healthy biol. effects. The microbiota has just been started to be considered as a metabolic organ, hence contributing to the metab. of phenolic compds. and, consequently, to their bioavailability and the biol. effects displayed by them. This review aimed to compile information regarding interaction of anthocyanins with the microbiota, from two perspectives: (i) identification of their colonic metabolites as potential bioactive mols. and (ii) their role as prebiotic agents. These perspectives are key points in anthocyanin metabolomics. Several metabolites have been identified after anthocyanin consumption with potential health benefits, in particular phenolic acids and simple phenols. On the other hand, microbiota modulation is closely related to several physiol. impairments, and its modulation has been considered as a possible mechanism by which phenolic compds. may exert their effect.
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      Walle, T.; Browning, A. M.; Steed, L. L.; Reed, S. G.; Walle, U. K. Flavonoid glucosides are hydrolyzed and thus activated in the oral cavity in humans. J. Nutr. 2005, 135 (1), 48– 52,  DOI: 10.1093/jn/135.1.48
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      Flavonoid glucosides are hydrolyzed and thus activated in the oral cavity in humans
      Walle, Thomas; Browning, Alyson M.; Steed, Lisa L.; Reed, Susan G.; Walle, U. Kristina
      Journal of Nutrition (2005), 135 (1), 48-52CODEN: JONUAI; ISSN:0022-3166. (American Society for Nutritional Sciences)
      Increasing epidemiol. evidence supports the view that dietary flavonoids have protective roles in oral diseases, including cancer. However, the dietary forms of flavonoids, the flavonoid glycosides, must first be hydrolyzed to the aglycons, which is thought to occur mainly in the intestine. In the present study we tested whether this hydrolytic activity occurs in the oral cavity. Saliva was collected from human subjects, incubated with flavonoid glycosides, and analyzed for aglycon formation by HPLC. When quercetin 4'-glucoside or genistein 7-glucoside was incubated with human saliva, hydrolysis to quercetin and genistein, resp., was detected within minutes. Studies of addnl. flavonoid glycosides demonstrated that glucose conjugates were rapidly hydrolyzed, but not conjugates with other sugars, i.e., rutin, quercitrin, and naringin. In a limited study of 17 subjects, the interindividual variability in the hydrolysis of genistein 7-glucoside was >20-fold. This supports the contention that salivary hydrolysis of certain flavonoid glucosides may be important in some individuals but not in others. Support for a bacterial contribution to this hydrolysis was obtained from the inhibitory effect of antibacterials in vivo and in vitro and from expts. with subcultured oral bacterial colonies. However, cytosol isolated from oral epithelial cells was also capable of effective hydrolysis. Dietary flavonoid glucosides may thus be hydrolyzed in the oral cavity by both bacteria and shedded epithelial cells to deliver the biol. active aglycons at the surface of the epithelial cells. The aglycons quercetin and genistein both potently inhibited proliferation of oral cancer cells. The large interindividual variability in this hydrolytic activity may be a factor that should be taken into consideration in future studies.
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      Muñoz-Gonzalez, C.; Cueva, C.; Angeles Pozo-Bayon, M.; Victoria Moreno-Arribas, M. Ability of human oral microbiota to produce wine odorant aglycones from odourless grape glycosidic aroma precursors. Food Chem. 2015, 187, 112– 9,  DOI: 10.1016/j.foodchem.2015.04.068
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      Cueva, C.; Sanchez-Patan, F.; Monagas, M.; Walton, G. E.; Gibson, G. R.; Martin-Alvarez, P. J.; Bartolome, B.; Moreno-Arribas, M. V. In vitro fermentation of grape seed flavan-3-ol fractions by human faecal microbiota: changes in microbial groups and phenolic metabolites. FEMS Microbiol. Ecol. 2013, 83 (3), 792– 805,  DOI: 10.1111/1574-6941.12037
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      In vitro fermentation of grape seed flavan-3-ol fractions by human faecal microbiota: changes in microbial groups and phenolic metabolites
      Cueva, Carolina; Sanchez-Patan, Fernando; Monagas, Maria; Walton, Gemma E.; Gibson, Glenn R.; Martin-Alvarez, Pedro J.; Bartolome, Begona; Moreno-Arribas, M. Victoria
      FEMS Microbiology Ecology (2013), 83 (3), 792-805CODEN: FMECEZ; ISSN:0168-6496. (Wiley-Blackwell)
      With the aim of investigating the potential of flavan-3-ols to influence the growth of intestinal bacterial groups, we have carried out the in vitro fermn., with human faecal microbiota, of two purified fractions from grape seed ext. (GSE): GSE-M (70% monomers and 28% procyanidins) and GSE-O (21% monomers and 78% procyanidins). Samples were collected at 0, 5, 10, 24, 30 and 48 h of fermn. for bacterial enumeration by fluorescent in situ hybridization and for anal. of phenolic metabolites. Both GSE-M and GSE-O fractions promoted growth of Lactobacillus/Enterococcus and decrease in the Clostridium histolyticum group during fermn., although the effects were only statistically significant with GSE-M for Lactobacillus/Enterococcus (at 5 and 10 h of fermn.) and GSE-O for C. histolyticum (at 10 h of fermn.). Main changes in polyphenol catabolism also occurred during the first 10 h of fermn.; however, no significant correlation coeffs. (P > 0.05) were found between changes in microbial populations and precursor flavan-3-ols or microbial metabolites. Together, these data suggest that the flavan-3-ol profile of a particular food source could affect the microbiota compn. and its catabolic activity, inducing changes that could in turn affect the bioavailability and potential bioactivity of these compds.
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      Aragonès, G.; Danesi, F.; Del Rio, D.; Mena, P. The importance of studying cell metabolism when testing the bioactivity of phenolic compounds. Trends Food Sci. Technol. 2017, 69, 230– 242,  DOI: 10.1016/j.tifs.2017.02.001
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      The importance of studying cell metabolism when testing the bioactivity of phenolic compounds
      Aragones, Gerard; Danesi, Francesca; Del Rio, Daniele; Mena, Pedro
      Trends in Food Science & Technology (2017), 69 (Part_B), 230-242CODEN: TFTEEH; ISSN:0924-2244. (Elsevier Ltd.)
      Metabolic transformations of phenolic compds. in in vitro models may alter the structure of mols. present in the cell media, entailing the existence of a dynamic scenario and conditioning the bioactivity of the tested compds. Nevertheless, most of the bioactivity studies carried out with cells do not evaluate these potentially confounding reactions. The metabolic fate of phenolic compds. in contact with different cell lines has been reviewed to highlight the importance of cell metab. when testing the biol. properties of phenolic metabolites. The review is divided in two main blocks. The first one summarizes the transformation of the main groups of phenolic compds. by intestinal and hepatic cells. The second one is devoted to the transformation of some phenolic metabolites in cell models corresponding to peripheral tissues. Some practical recommendations are also provided to assist future researchers in the field. The occurrence of newly-formed metabolites in cell expts. seems to be cell type- and compd.-specific. Metabolic reactions occurring in cell exptl. models may represent a limiting or promoting step to elicit bioactivity. They may be relevant for understanding the mols. and mechanisms responsible for the biol. effects of phenolic metabolites. Therefore, the anal. of the cell media/lysates used in bioactivity expts. is a paramount step to fully clarify the real metabolites behind the obsd. bioactivity. Future in vitro research should take into account the assessment of cellular metab. of phenolic bioactives.
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    58. 58
      Mena, P.; González de Llano, D.; Brindani, N.; Esteban-Fernández, A.; Curti, C.; Moreno-Arribas, M. V.; Del Rio, D.; Bartolomé, B. 5-(3′,4′-Dihydroxyphenyl)-γ-valerolactone and its sulphate conjugates, representative circulating metabolites of flavan-3-ols, exhibit anti-adhesive activity against uropathogenic Escherichia coli in bladder epithelial cells. J. Funct. Foods 2017, 29, 275– 280,  DOI: 10.1016/j.jff.2016.12.035
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      5-(3',4'-Dihydroxyphenyl)-γ-valerolactone and its sulphate conjugates, representative circulating metabolites of flavan-3-ols, exhibit anti-adhesive activity against uropathogenic Escherichia coli in bladder epithelial cells
      Mena, Pedro; Gonzalez de Llano, Dolores; Brindani, Nicoletta; Esteban-Fernandez, Adelaida; Curti, Claudio; Moreno-Arribas, Maria Victoria; Del Rio, Daniele; Bartolome, Begona
      Journal of Functional Foods (2017), 29 (), 275-280CODEN: JFFOAX; ISSN:1756-4646. (Elsevier Ltd.)
      Urinary tract infections (UTI) are mostly caused by uropathogenic Escherichia coli (UPEC). Cranberry-based products have shown preventive effects against UTI, and this has been partially attributed to their A-type proanthocyanidin content. However, recent evidence reports phenyl-γ-valerolactones as the most relevant urinary metabolites of cranberry procyanidins, and candidates these compds. as plausible responsible for the protective effects of cranberries against UTI. This paper studied the inhibition of the adherence of UPEC ATCC53503 to T24 bladder epithelial cells by physiol. concns. of differently sulfated dihydroxyphenyl-γ-valerolactones. Moreover, the transformations of these mols. in the cell media were evaluated by UHPLC-MSn. All dihydroxyphenyl-γ-valerolactone derivs. showed anti-adhesive activity at 100 μM, while 5-(3'-hydroxyphenyl)-γ-valerolactone-4-O-sulfate also showed neuro-protective effects at 50 μM. Some compds. underwent extensive metab. during cell incubation, mainly deconjugation of sulfate moieties and opening of the lactone ring. These results shed light on the flavan-3-ol metabolites behind the prophylactic effect of cranberries against UTI.
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      Moridani, M. Y.; Scobie, H.; Jamshidzadeh, A.; Salehi, P.; O’Brien, P. J. Caffeic acid, chlorogenic acid, and dihydrocaffeic acid metabolism: glutathione conjugate formation. Drug Metab. Dispos. 2001, 29 (11), 1432– 1439
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      Mallery, S. R.; Budendorf, D. E.; Larsen, M. P.; Pei, P.; Tong, M.; Holpuch, A. S.; Larsen, P. E.; Stoner, G. D.; Fields, H. W.; Chan, K. K.; Ling, Y.; Liu, Z. Effects of human oral mucosal tissue, saliva, and oral microflora on intraoral metabolism and bioactivation of black raspberry anthocyanins. Cancer Prev. Res. 2011, 4 (8), 1209– 21,  DOI: 10.1158/1940-6207.CAPR-11-0040
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      Effects of human oral mucosal tissue, saliva, and oral microflora on intraoral metabolism and bioactivation of black raspberry anthocyanins
      Mallery, Susan R.; Budendorf, Deric E.; Larsen, Matthew P.; Pei, Ping; Tong, Meng; Holpuch, Andrew S.; Larsen, Peter E.; Stoner, Gary D.; Fields, Henry W.; Chan, Kenneth K.; Ling, Yonghua; Liu, Zhongfa
      Cancer Prevention Research (2011), 4 (8), 1209-1221CODEN: CPRACC; ISSN:1940-6207. (American Association for Cancer Research)
      Our oral cancer chemoprevention trial data implied that patient-specific differences in local retention and metab. of freeze-dried components of black raspberries (BRB) affected therapeutic responsiveness. Subsequent studies have confirmed that anthocyanins are key contributors to BRB's chemopreventive effects. Consequently, functional assays, immunoblotting, and immunohistochem. analyses to evaluate levels and distribution of BRB anthocyanin-relevant metabolic enzymes in human oral tissues were conducted. Liq. chromatog./tandem mass spectrometry (LC/MS-MS) analyses of time course saliva samples collected following BRB rinses were conducted to assess local pharmacokinetics and compare the capacities of three different BRB rinse formulations to provide sustained intraoral levels of anthocyanins. Protein profiles showed the presence of key metabolic enzymes in all 15 oral mucosal tissues evaluated, whereas immunohistochem. confirmed these enzymes were distributed within surface oral epithelia and terminal salivary ducts. β-Glucosidase assays confirmed that whole and microflora-reduced saliva can deglycosylate BRB anthocyanins, enabling generation of the bioactive aglycon, cyanidin. LC/MS-MS analyses showed retention of parent anthocyanins and their functional, stable metabolite, protocatechuic acid, in saliva for up to 4 h after rinsing. Furthermore, postrinse saliva samples contained glucuronidated anthocyanin conjugates, consistent with intracellular uptake and phase II conversion of BRB anthocyanins into forms amenable to local recycling. Our data show that comparable to the small intestine, the requisite hydrolytic, phase II and efflux transporting enzymes necessary for local enteric recycling are present and functional in human oral mucosa. Notably, interpatient differences in anthocyanin bioactivation and capacities for enteric recycling would impact treatment as retention of bioactivated chemopreventives at the target site would sustain therapeutic effectiveness.
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      https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BC3MXhtFGmtrfP&md5=b36d2601d132daf0a3ca2bf8c18cbe42
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