Open access peer-reviewed chapter

Phenolic Compounds in Legumes: Composition, Processing and Gut Health

Written By

Mayra Nicolás-García, Cristian Jiménez-Martínez, Madeleine Perucini-Avendaño, Brenda Hildeliza Camacho-Díaz, Antonio Ruperto Jiménez-Aparicio and Gloria Dávila-Ortiz

Submitted: 06 April 2021 Reviewed: 30 April 2021 Published: 29 June 2021

DOI: 10.5772/intechopen.98202

From the Edited Volume

Legumes Research - Volume 2

Edited by Jose C. Jimenez-Lopez and Alfonso Clemente

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Abstract

Gut health is fundamental for human well-being and prevents chronic degenerative diseases and is influenced by the interaction between gut microbiota and food components. In recent years, interest in phenolic compounds has increased due to their health benefits such as antioxidant, antidiabetic, antimicrobial, anti-atherosclerotic, anti-inflammatory, anticarcinogenic, cardio- and neuro-protective properties. Legumes are an essential source of phytochemicals, particularly flavonoids and phenolic acids, distributed mainly in the seed coat, and have been reported to exhibit multiple biological effects. Flavonoids present in legumes have been shown to regulate metabolic stability and membrane transport in the intestine, thus improving bioavailability. Seed processing such as cooking allows the release of phenolic compounds, improving polyphenols digestion and absorption at the intestinal level, maintaining their protective capacity in the oxidative process at the cellular level, and modulating the gut microbiota. All these actions improve gut health, avoiding diseases like irritable bowel syndrome, inflammatory bowel disease, obesity, diabetes, colitis, and colorectal cancer. The effect of the consumption of legumes such as chickpea, pea, and bean, as well as the contribution of phenolic compounds to gut health, will be reviewed in this study.

Keywords

  • Legumes
  • biological effects
  • phenolic compounds
  • seed processing
  • chronic degenerative diseases
  • gut microbiota
  • gut health

1. Introduction

Eating habits are an important factor in the structure, formation, function, and modulation of the gut microbiota, which plays a crucial role in health; environmental factors, antibiotics, and lifestyle also contribute to the dysbiosis of the gut microbiota responsible for gastrointestinal diseases, like colon cancer. Several studies have shown that the gut has a greater impact than food processing and nutrient absorption. Gut health is a function of the gut barrier and gut microbiota essential elements for better health [1, 2, 3, 4, 5, 6].

Plants contribute diverse bioactive compounds to the diet [7, 8], including phenolic compounds. Legumes are part of the basic foods with great nutritional relevance due to their content of diverse phenolic compounds that promote health [5, 9]. These compounds are distributed in the whole seed and are mainly responsible for the seed coat color that depends on the composition and concentration [10, 11, 12, 13, 14]. The potential health benefits of phenolic compounds in the diet depend on their absorption and metabolism, which in turn are determined by their structure, including their conjugation with other phenols, degree of glycosylation/acylation, molecular size, and solubility [9, 15, 16, 17]. During seed processing, phenolic compounds can undergo various changes, altering their antioxidant activity [18, 19].

However, the presence of phenolic compounds and their mechanisms of action in preventing colon cancer or inflammation are probably mediated by the functional composition of the gut microbiota [20, 21, 22]. Epidemiological studies have confirmed that regular consumption of legumes has been associated with lower risk due to immunomodulatory effects and prevention of chronic and metabolic diseases, such as cardiovascular diseases, diabetes, cancer, and obesity, in addition to improving gut health [11, 16, 20, 23, 24].

During the absorption of phenolic compounds, like hydroxycinnamic acids (p-coumaric, caffeic, and ferulic) in free and conjugated forms, they are metabolized by the gut microbiota (e.g., genera Bifidobacterium, Lactobacillus, and Escherichia) are able to release them [8]. Moreover, flavonoid glycosides are deconjugated by microbial glucuronidases and sulfatases in the colon, releasing aglycones such as quercetin, myricetin, and kaempferol that can be metabolized by different genera of intestinal bacteria, including Clostridium sp., Eubacterium sp., Enterococcus sp., among others, to form hydroxyphenylacetic and hydroxyphenylpropionic acids as major metabolites leading to increased bioavailability of phenolic compounds [24].

Chickpea, pea, and bean seeds are among the most widely consumed food legumes worldwide. The genus Cicer comprises about 44 species. The chickpea (Cicer arietinum L.) has two commercial varieties ‘Desi’ and ‘Kabuli’ and their characteristics vary according to geographical distribution, shape, size, and color. The color of the Desi variety is dark in comparison with the Kabuli chickpea, which has a fine, light-colored covering and is the most widely consumed [20, 23].

Pisum sativum L., commonly known as pea, represents one of the oldest and most widespread cultivated legumes worldwide due to its wide availability, low cost, and high nutritional value [1, 16], they are small seeds with a green or yellow spherical shape. Quality characteristics depend on biological factors between the environment and genetics [25]. Another important legume in food is the genus Phaseolus, which includes species such as P. vulgaris, P. lunatus, P. coccineus, P. acutifolius, and P. dumosus; among these, the most cultivated in Mexico is the common bean (P. vulgaris) that has more than 70 varieties grouped according to their color in black, yellow, red, brown, white, purple, and pinto [14, 26, 27].

Phenolic compounds constitute an important group of secondary plant metabolites and influence the diversity and quantity of gut microbial species, allotting prebiotic effects to phenolic compounds, mainly flavonoids involved in modulating the taxonomic composition of the gut microbiota, increasing the relative abundance of beneficial species, and inhibiting the proliferation of bacterial species associated with negative implications [7, 24].

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2. Phenolic compounds in chickpea, pea, and common bean: chemistry, distribution, and beneficial effects

Legumes are an excellent source of phytochemicals, including phenolic acids, flavonols, flavones, flavanols, flavanones, isoflavones, anthocyanins, tannins, and other phenolics [14, 16, 28, 29]. The structure of polyphenols and their composition and interaction in a food matrix are important determinants of their bioavailability and bioactivity [12, 15, 30]. Figure 1 shows the structures of phenolic compounds present in chickpea, pea, and bean. Differences in the phenolic profile of various legumes influence the specific health benefits. The presence of phenolic acids and flavonoids in legumes such as chickpea, pea, and beans have been reported in different units of concentration and are presented in Table 1.

Figure 1.

Main phenolic compounds in legumes [20, 28, 31].

CompoundConcentration (DW)References
ChickpeaPeaBean
Phenolic acids
p-Hydroxybenzoic acid10.5b/0.08–1.63c588.94a0.30-16.30b[20, 31, 32, 33, 34]
Protocatechuic acid358.9b/0.51c426.15a/0.89-2.25d0.42-37.36b/170-177c[20, 31, 32, 33, 35, 36, 37]
Syringic acid222.1b/0.63–1.95cnd10.60-11.40c[20, 31, 34, 38]
Vanillic acid80.8b/0.34c536.67a618.44b[20, 31, 33, 36, 39]
Gallic acid40.2b/4.66c218.45a/9.08-29.95d0.15–21.30c[20, 31, 33, 34, 35, 40]
Ellagic acid0.43c433.87a/899.19c4.3-18.08b[20, 33, 41, 42, 43]
Caffeic acid0.11c146.11a/0.20–0.92d3.08-11.70b[20, 33, 35, 36, 42]
Chlorogenic acidnd742.28a/0.57–1.27d3.03-33.38b/6.63-46.1c[33, 34, 35, 36, 37, 40, 42, 44]
p-coumaric acid0.11c462.93a/7.78c/9.0-16.2d0.40-1.90b/0.74c[20, 33, 40, 41, 44, 45, 46]
Ferulic acid0.90b/0.22c788.29a/1.38-3.44d0.91-11.00b[20, 31, 33, 35, 36, 44, 46]
Sinapic acid7.81b/0.12dnd2.9-86.27b[20, 31, 32, 39, 46]
Flavonoids
Quercetinnd56.90c/0.12-1.51d0.8-30.88b/0.30-1.31c[33, 34, 35, 39, 40, 44, 46]
Quercetrinnd256.26c1.07c[33, 40]
Myricetinndnd1.99–5.98b[43, 44, 46]
Kaempferol0.09b19.79c2.51b/0.13c[33, 40, 44, 46, 47]
Rutin0.101c83.01c/0.26-1.31d0.20-119.70c[33, 34, 35, 37, 40]
Naringeninnd24.59cnd[33]
Naringinnd201.41c2.35c[33, 40]
Hesperidinnd605.94c8.10c[33, 40]
Hespirtinnd158.29c0.56c[33, 40]
Catechinnd93-2303d10.05-78.34b[32, 39, 43, 44, 45]
Epicatechinnd1.03–13.02d10.90-34.48b[35, 42, 43]
Luteolin1.56b3.24-8.57d2.41c[31, 35, 40]
Apigeninnd14.31cnd[33]
Genistein0.06end3.64-4.74c[37, 48]
Daidzein0.12endnd[48]
Formononetin0.02b/0.10end35.94-163.34b[43, 47, 48]
Biochanin A0.78bndnd[47]
Biochanin glucoside0.08endnd[48]
Biochanin A derivative3.31–5.25bndnd[47]

Table 1.

Polyphenols reported in chickpea (C. arietinum), pea (P. sativum) and common bean (P. vulgaris) seeds.

ppm.


μg/g.


mg/100 g.


mg/kg.


mg/g.


DW: Dry weight, nd: not detected.

Phenolic compounds are present in soluble and insoluble forms. Therefore, it is very important to optimize the polyphenols extraction process [9, 10]. Most of the phenolic compounds associated with whole seed are in insoluble bound forms, mainly phenolic acids, linked covalently to cell wall structural components like cellulose, hemicellulose, lignin, and pectin [14, 20, 30, 45].

Chickpea contains several phenolic compounds, including lignans (secoisolariciresinol, pinoresinol, and lariciresinol), isoflavones, flavonoids, phenolic acids, and anthocyanins [20, 49]. Besides, it has significant amounts of flavonoids, especially isoflavones, the main ones being biochanin A and formononetin, to a lesser extent genistein and daidzein [5, 9, 12, 47].

The main compounds in peas are glycosylated flavonols, condensed tannins, as well as hydroxybenzoic and hydroxycinnamic acids, such as quercetin, kaempferol, luteolin, apigenin, flavan-3-ols, apigenin-7-glucoside, quercetin-3-rhamnoside, kaempferol-3-glucoside, flavonols, flavones, and stilbenes; the main compounds identified in the whole seed are hesperidin and catechin [26, 47]. In beans, phenolic acids and flavonoids represent 50% of the total content of phenolic compounds like vanillic, ferulic, 4-hydroxybenzoic, sinapic acids; quercetin, myricetin, and catechin are the major phenolic acids contained in bean seeds and determine the seed color [10, 14, 28].

The phenolic composition of legumes has been particularly interesting for metabolic health because of their protection against oxidative damage [45]. Phenolic compounds constitute an important group of secondary plant metabolites, important for health by preventing multiple degenerative conditions in the body [16]. These compounds are biologically active and have been associated with antidiabetic, anticarcinogenic, antihypertensive, antimutagenic, antioxidant, antimicrobial, anti-inflammatory, anticholesterolemic, cardioprotective, immunostimulant, and anti-angiogenic properties [11, 14, 16, 20, 21, 29, 35, 41, 49, 50].

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3. Impact of processing on phenolic compounds

Processing of legumes may result in an increase or decrease in the content of phenolic compounds. During processing, phenolic compounds may undergo various changes, altering the antioxidant activity of the products. Changes in phenolic content depend on the species, variety, and processing conditions [12, 18, 22]. Processes such as soaking, cooking, extrusion, germination, fermentation, and roasting improve the release of bound phenolic compounds, which influences the sensory properties of the seeds [51, 52, 53, 54].

During processing, a reduction in the content of condensed tannins has been reported. In legumes, soaking has been found to decrease tannic acid content by approximately 20%, and germination reduces tannin content by 50%. The decrease of phenolic compounds during soaking and cooking may be due to several factors during the heat treatment, such as 1) polyphenol-protein interactions that decrease the extraction capacity, 2) the formation of tannin complexes with other water-soluble components, and 3) the lixiviation and thermal degradation of phenolic compounds [12, 14, 30]. However, unlike traditional processing or pressure cooking, the extrusion process is carried out in the absence of effluents, so the impact on phenolic content is less [52, 55, 56]. Arribas et al. [55] observed that extrusion does not affect the phenolic groups to the same extent; they reported that the anthocyanin content in extruded pea decreased from 4 to 50% as opposed to the flavonol content, which increased approximately three times.

On the other hand, the germination process increases bioactive compounds, like phenolic compounds, improving the seeds functionality. The increase is attributed to biosynthesis through the Shikimate pathway and the release of phenolic compounds. During germination, enzymatic reactions are activated, such as the enzyme phenylalanine ammonia lyase, which promote the phenolic compounds’ biosynthesis. The endogenous esterases action allows the liberation of hydroxycinnamic acids linked to arabinoxylans and lignin in the cell wall [20, 57, 58]. Nevertheless, changes in isoflavones during this process may be related to genetic regulation. They may be induced by the metabolic pathways of naringenin chalcone and isoliquiritigenin, the precursors of isoflavonoids, present in legumes. Therefore, germination is an efficient alternative to increase antioxidant activity and has been used in legumes such as chickpeas, peas, and beans [9, 12, 48, 50]. Domínguez-Arispuro et al. [20] observed that the germination process in chickpeas induced an increase of 97 and 111% of the total phenolic and flavonoid content, respectively, as compared to the raw seed. Moreover, formononetin and biochanin contents of 0.10 and 0.18 mg/g, respectively, have been reported in raw chickpea; during a 10-day germination process, they increased to 1.42 and 2.10 mg/g respectively [48].

The fermentation process has been reported to cause an increase in free radical scavenging capacity. Changes in phenolic composition are associated with sensory, nutritional, and biochemical properties and depend on fermentation conditions such as optimal time and temperature to avoid a further reduction, mainly in tannin content [53, 59, 60]. Bulbula & Urga [53] reported the effect of different traditional processing methods on tannins in chickpea, noting that during boiling, toasting, and fermentation at 0 h, there are no differences from raw seed beans. However, during fermentation for 24, 48, 72 h and chickpea germination, tannin content decreased by 3.1, 14.4, 18.5, and 43.4%, respectively. The reduction of tannins during germination is generally attributed to enzymatic hydrolysis by polyphenolase.

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4. Impact of phenolic compounds on the gut health and its relationship with human health

The gut microbiota plays an important role in food digestion, immunity, and other metabolic functions; its composition is influenced by endogenous and environmental factors such as age, diet, lifestyle, antibiotic intake, and xenobiotics. Optimal gut health depends on the microbial community structure, a balanced composition of gut microbiota, an epithelial barrier, and an intact host mucosa; therefore, a disorder of these components can lead to the development of intestinal diseases such as obesity, inflammatory bowel disease, and colon cancer [1, 2, 3, 6, 7, 21, 22, 24, 49, 61].

Legumes are composed of bioactive compounds, such as phenolic compounds, capable of modifying the physiological basal function within the intestinal microenvironment affecting the microbiota and epithelial barrier, improving metabolic and gastrointestinal health, enhancing resistance to colonization by pathogens, and exerting an impact on the gut microbiota. These actions lead to decrease the severity of diseases associated with the intestine due to their chemopreventive effects. However, not all polyphenols support gastrointestinal integrity equally, and their benefits depend on chemical structure and phenolic concentration [12, 21, 31, 49, 62]. Isoflavones, such as biochanin A, have been reported to improve gut health by exerting antioxidant and anti-inflammatory effects [12, 20, 21]. On the other hand, the effect of formononetin in an acute colitis model in mice induced by dextran sulfate sodium has been evaluated, observing an attenuation of colitis. This effect may be due to the inhibition of the NLRP3 immamasome pathway by the action of formononetin [9].

Bian et al. [2] suggest that kaempferol has a protective effect on the secretion of interleukin-8 (IL-8) and the barrier dysfunction of the Caco-2 monolayer in the lipopolysaccharide-induced epithelial-endothelial co-culture model. This effect is due to the inhibition of the nuclear factor-kappa B (NF-κB) signaling pathway, which allows the reduction of inflammatory bowel disease. Also, caffeic acid reduces the secretion of pro-inflammatory cytokines, including interleukin-6 (IL-6), tumor necrosis factor-alpha (TNF-𝛼), and IFN𝛾, and colonic infiltration of CD3+ T cells, CD177+ neutrophils, and F4/80+ macrophages by inhibiting the activation of the NF-𝜅B signaling pathway [63]. Naringin is a flavonoid that has a beneficial effect on intestinal disorders. Liu et al. [64] showed that naringin (50 μM) protects the integrity of rat intestinal microvascular endothelial cell monolayer barriers against TNF-α-induced disruption, preventing TNF-α-induced apoptosis and suppressing cell migration, and avoiding gut-vascular barrier disruption. Moreover, the proanthocyanidins or condensed tannins have been reported to have bioactive properties like anti-inflammatory and antimicrobial, causing a reduction in intestinal inflammation and promoting the growth of Lactobacillus spp. and Bifidobacteria spp. [1, 62].

Recent animal studies have shown that chickpeas consumption improves gut health by inhibiting the proliferation of cancer cells, attenuating inflammation, modulating the composition and activity of the microbiome, promoting epithelial barrier integrity, mucus production, and antimicrobial defenses [49, 65]. In addition, the quantitative structure–activity relationship on the cytotoxic effect of phenolic compounds have been studied. The p-hydroxybenzoic acid present in P. sativum exhibits strong cytotoxic activity in the colon carcinoma (HCT116) cell line [33]. Additional clinical evidence suggests that bean intake may reduce the incidence of developing advanced colorectal adenoma in humans [66]. Chen et al. [67] noted that cyanidin-3-O-glucoside protects against intestinal mucosal damage caused by 3-chloro-1, 2-propanediol (3-MCPD), a food contaminant. Figure 2 shows the prebiotic effect of anthocyanins on the gut microbiota.

Figure 2.

The potential prebiotic effect of anthocyanins on gut microbiota and obesity. SCFA: Short-chain fatty acids; FIAF: Fasting-induced adipose factor; LPS: Lipopolysaccharide; ZO-1: Zonula occludens-1; IR: Insulin resistance. Anthocyanins and metabolites formed in the intestine change the composition of the gut microbiota. This is associated with restored tight-junction protein (ZO-1 and occludin) distribution, and localization. Hence, the gut permeability is decreased, and plasma lipopolysaccharide (LPS) levels (metabolic endotoxemia) are lowered, improving low-grade inflammation and obesity-related comorbidities. Anthocyanins decrease transcription factor NF-kB activity in the cell nucleus by decreasing gene expression of inflammatory cytokines, exerting their anti-inflammatory action. Anthocyanins have the ability to promote the growth of Bifidobacterium spp., which increases the intestinal production of FIAF that inhibits fat storage in the host. Bifidobacterium spp. degrade SCFA; propionate stimulates mucus secretion and contributes to thickening of the mucus layer. At the same time, reduced mucus layer thickness favors microbiota encroachment. The figure is taken from [15].

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5. Phenolic compounds during gastrointestinal digestion: bioaccessibility and bioavailability

Bioaccessibility is defined from a nutritional point of view as the fraction of compounds liberated from the food matrix within the human gastrointestinal tract and available for intestinal absorption. The gastrointestinal tract is prone to oxidative stress due to its function as a primary digestive system and exposure to various stimuli [15, 29, 67]. The bioaccessibility and bioavailability of several phenolic compounds have been studied, noting that the aglycones in isoflavones are more bioavailable than their conjugated counterparts [9]. The absorption and bioavailability of phenolic compounds are commonly affected by low solubility, low permeability, and low stability in the gastrointestinal tract [29]. Some researchers have suggested that 5–20% of the total polyphenol content in legumes can be absorbed. The preventive action provided by these compounds depends on bioaccessibility. However, in the case of chronic diseases, such as stomach and colorectal cancer, they do not depend on the polyphenols bioaccessibility; still, gut microbiota can increase the bioavailability of the phenolic content of foods and quadruple their antioxidant activity [9, 12, 15, 29, 67].

5.1 Oral cavity absorption

During oral digestion, the food matrix is broken down, allowing phenolic compounds and other nutrients to be released into the environment due to enzymatic hydrolysis by salivary α-amylase. However, the decrease in polyphenols such as condensed tannins during mastication is due to the interaction with salivary proteins resulting in insoluble aggregates [50]. Luzardo-Ocampo et al. [68] indicated that the antioxidant activity of bean methanolic extracts during in vitro gastrointestinal digestion increases in the mouth stage due to a higher release of certain polyphenols such as catechin, chlorogenic acid, and vanillin. As gastrointestinal digestion progresses, antioxidant activity is increased until it reaches the large intestine, where it decreases.

5.2 Gastric absorption

Polyphenols are very poorly absorbed after ingestion and remain in the gastrointestinal tract, where they influence digestive enzymes activity, inhibiting crucial enzymes involved in the digestion of starch (α-amylase), lipids (pancreatic lipase), and protein digestibility (pepsin and trypsin). Digestibility is influenced by the polyphenol’s interaction with food and endogenous proteins, like digestive enzymes, salivary proteins, gastric and intestinal mucosa, and other endogenous proteins on the luminal side of the intestinal tract [16, 69, 70]. Studies with in vitro simulation revealed that during gastric digestion (pH 1.2–2.0 in the presence of pepsin), there is a decrease in the recovery of phenolic compounds because they can interact with the pectin present in the food [29]. However, the presence of (+)-catechin has been evidenced in the stomach stage due to resistance to the acid environment [68].

5.3 Intestinal absorption

Polyphenols are not completely absorbed in the small intestine (5–10%). More than 90% enter the large intestine and are fermented by the human colon microbiota interacting with microorganisms (10–14 bacterial cells) and enzymes (α-L-rhamnosidase and β-D-glucosidase). Fermentation facilitates the liberation and absorption of insoluble bound phenolics involved in colorectal cancer prevention. The degradation of phenolic acids by enteric bacterial or chemical conversions may produce other metabolites, including protocatechuic acid, syringic acid, vanillic acid, phloroglucinol aldehyde, phloroglucinol acid, and gallic acid [3, 9, 15, 20, 21, 24, 30, 63, 69].

Phenolic compounds are catabolized by the gut microbiota, originate common phenolic (e.g., daidzein to equol, flavan-3-ols to valerolactones, and ellagitannins to urolithins) intermediates as in phenylpropionic, phenylacetic, and benzoic acids with different degrees of hydroxylation [17]. The flavonoids present in bound form (glycosides) and in free form (aglycones) are changed during digestion; a low fraction of these glycosides can be enzymatically hydrolyzed to aglycones in the small intestine, causing these aglycones to be more hydrophobic compared to the original glycosides. Aglycones are absorbed by epithelial cells through passive diffusion and then transported to the liver, where they will be metabolized. However, flavonoid glycosides are hardly absorbed in the small intestine due to their hydrophilic nature and reach the large intestine intact, where they will be metabolized by the gut microbiota [24].

During intestinal digestion, polyphenols such as anthocyanins, phenolic acids, catechin, quercetin, resveratrol, and rutin are unstable in the alkaline environment intestinal fluid (pH 6.8–8.0) due to their degradation [29]. The main phenolic acids absorbed in the small intestine are gallic, caffeic, and ferulic acids [63, 68]. Luzardo-Ocampo et al. [68] observed that phenolic acids in beans, like ferulic, chlorogenic, and vanillin, do not change their content during their passage through the small intestine, for 60–120 min, indicating their resistance to the intestinal enzymes and allowing them to arrive at the large intestine for fermentation. Milán-Noris et al. [12] observed that chickpea cooking increased intestinal absorption of the existent isoflavones. On the other hand, Cárdenas-Castro et al. [54] evaluated the bioaccessibility and in vitro release kinetics of phenolic compounds from two varieties of beans (Azufrado and Negro Jamapa). These authors reported that in cooked beans, the phenolic compounds showed 50% bioaccessibility, and 30% in cooked-fried beans, indicating that cooking did not modify the release kinetics of phenolic compounds during the first 60 min, being kaempferol-3-O-glucoside, quercetin-3-O-glucoside, and chlorogenic acid the main compounds released.

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6. Interactions of phenolic compounds with the gut microbiota: metabolism and modulation

The interaction between the gut microbiota and the diet components is fundamental to the promotion of gut health. Lignans, flavonoids, and other phenolic compounds present in legumes participate in the modulation of the host’s mucosal barrier integrity, attenuate the inflammatory process associated with colitis, and improve epithelial barrier integrity, aside from modulating fecal and cecal microbiota composition and providing beneficial effects against metabolic diseases like obesity. The interaction of gut microbiota and phenolic compounds, mainly anthocyanins, can implicate hydrolysis, demethylation, reduction, decarboxylation, dehydroxylation, or isomerization of compounds into simpler components to modulate absorption [15, 21, 49, 69]. Chlorogenic acid is poorly absorbed in the small intestine, but it has been shown that the bioavailability of this compound depends on the metabolism of the gut microflora. However, when this compound is metabolized in the colon, it modulates the colonic microbiota inducing a significant increase in the growth of Bifidobacterium spp. and Clostridium coccoides-Eubacterium rectale, revealing a potent antimicrobial activity by binding and permeabilizing the bacterial cell membrane [63]. On the other hand, it has been shown that phenolic compounds present in cooked chickpeas, like quercetin, daidzein, biochanin A, and formononetin, improved the integrity of the intestinal barrier by reducing its permeability and providing antioxidant and anti-inflammatory effects that promote gut health and decrease pathologies, like colitis [21, 49].

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7. Conclusion

The inclusion of legumes such as chickpeas, peas and beans in the diet has increased consumer health benefits due to their content of bioactive compounds such as phenolic compounds and other nutrients. During digestion, these compounds are not completely absorbed in the intestinal tract and are metabolized in the colon, increasing their bioaccessibility and bioavailability. These compounds have been shown to participate in the modulation of the gut microbiota, the epithelial barrier and resistance to pathogen colonization, improving gut health by inhibiting the proliferation of cancer cells through their chemopreventive effects. The impact of phenolic compounds on the gut microbiota suggests that the incorporation of legumes into the diet and the design of novel functional foods may improve human health by preventing the development of metabolic and gastrointestinal disorders, including irritable bowel syndrome, inflammatory bowel disease, obesity, diabetes, colitis, and colorectal cancer. However, further research should be conducted to understand the impact of phenolic compounds during digestion and gut microbiota modulation.

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Acknowledgments

The authors are grateful to the Instituto Politécnico Nacional, Mexico (SIP projects: 20181560, 20196640, and 20200291), and CONACyT project (241756).

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Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1. Martens, L. G., Nilsen, M. M., & Provan, F. Pea hull fibre: Novel and sustainable fibre with important health and functional properties. ECNU. 2017; 10: 139-148
  2. 2. Bian, Y., Dong, Y., Sun, J., Sun, M., Hou, Q ., Lai, Y., & Zhang, B. Protective effect of kaempferol on LPS-induced inflammation and barrier dysfunction in a coculture model of intestinal epithelial cells and intestinal microvascular endothelial cells. J. Agric. Food Chem. 2019; 68 (1): 160-167. https://doi.org/10.1021/acs.jafc.9b06294
  3. 3. Moles, L., & Otaegui, D. The impact of diet on microbiota evolution and human health. Is diet an adequate tool for microbiota modulation?. Nutrients, 2020; 12 (6): 1654. https://doi.org/10.3390/nu12061654
  4. 4. Wan, M. L., Ling, K. H., El-Nezami, H., & Wang, M. F. Influence of functional food components on gut health. Crit. Rev. Food Sci. Nutr. 2019; 59 (12): 1927-1936. https://doi.org/10.1080/10408398.2018.1433629
  5. 5. Cid-Gallegos, M. S., Sánchez-Chino, X. M., Juárez Chairez, M. F., Álvarez González, I., Madrigal-Bujaidar, E., & Jiménez-Martínez, C. Anticarcinogenic activity of phenolic compounds from sprouted legumes. Food Res. Int. 2020; 1-16. https://doi.org/10.1080/87559129.2020.1840581
  6. 6. Fassarella, M., Blaak, E. E., Penders, J., Nauta, A., Smidt, H., & Zoetendal, E. G. Gut microbiome stability and resilience: elucidating the response to perturbations in order to modulate gut health. Gut. 2021; 70 (3): 595-605. http://dx.doi.org/10.1136/gutjnl-2020-321747
  7. 7. Danneskiold-Samsøe, N. B., Barros, H. D. D. F. Q ., Santos, R., Bicas, J. L., Cazarin, C. B. B., Madsen, L., & Júnior, M. R. M. Interplay between food and gut microbiota in health and disease. Food Res. Int. 2019; 115: 23-31. https://doi.org/10.1016/j.foodres.2018.07.043
  8. 8. Zmora, N., Suez, J., & Elinav, E. You are what you eat: diet, health and the gut microbiota. Nat. Rev. Gastroenterol Hepatol. 2019; 16 (1): 35-56. https://doi.org/10.1038/s41575-018-0061-2
  9. 9. De Camargo, A. C., Favero, B. T., Morzelle, M. C., Franchin, M., Alvarez-Parrilla, E., de la Rosa, L. A., Vilar Geraldi, M., Maróstica Júnior, M. R., Shahidi, F., & Schwember, A. R. Is chickpea a potential substitute for soybean? Phenolic bioactives and potential health benefits. Int. J. Mol. Sci. 2019; 20 (11): 2644. https://doi.org/10.3390/ijms20112644
  10. 10. Singh, B., Singh, J. P., Kaur, A., & Singh, N. Phenolic composition and antioxidant potential of grain legume seeds: A review. Food Res Int. 2017; 101: 1-16. https://doi.org/10.1016/j.foodres.2017.09.026
  11. 11. Awika, J. M., Rose, D. J., & Simsek, S. Complementary effects of cereal and pulse polyphenols and dietary fiber on chronic inflammation and gut health. Food Funct. 2018; 9 (3): 1389-1409. https://doi.org/10.1039/C7FO02011B
  12. 12. Milán-Noris, A. K., Gutiérrez-Uribe, J. A., Santacruz, A., Serna-Saldívar, S. O., & Martínez-Villaluenga, C. Peptides and isoflavones in gastrointestinal digests contribute to the anti-inflammatory potential of cooked or germinated desi and kabuli chickpea (Cicer arietinum L.). Food Chem. 2018; 268: 66-76. https://doi.org/10.1016/j.foodchem.2018.06.068
  13. 13. Fahim, J. R., Attia, E. Z., & Kamel, M. S. The phenolic profile of pea (Pisum sativum): a phytochemical and pharmacological overview. Phytochem. Rev. 2019; 18 (1): 173-198. https://doi.org/10.1007/s11101-018-9586-9
  14. 14. Nicolás-García, M., Perucini-Avendaño, M., Jiménez-Martínez, C., Perea-Flores, M. J., Gómez-Patiño, M. B., Arrieta-Báez, D., & Dávila-Ortiz, G. Bean phenolic compound changes during processing: chemical interactions and identification. J. Food Sci. 2021; 83 (3): 643-655. https://doi.org/10.1111/1750-3841.15632
  15. 15. Jamar, G., Estadella, D., & Pisani, L. P. Contribution of anthocyanin-rich foods in obesity control through gut microbiota interactions. BioFactors, 2017; 43 (4): 507-516. https://doi.org/10.1002/biof.1365
  16. 16. Guo, F., Xiong, H., Wang, X., Jiang, L., Yu, N., Hu, Z., Sun, Y., & Tsao, R. Phenolics of green pea (Pisum sativum L.) hulls, their plasma and urinary metabolites, bioavailability, and in vivo antioxidant activities in a rat model. J. Agric. Food Chem. 2019; 67 (43): 11955-11968. https://doi.org/10.1021/acs.jafc.9b04501
  17. 17. Pei, R., Liu, X., & Bolling, B. Flavonoids and gut health. Curr. Opin. Biotechnol. 2020; 61: 153-159. https://doi.org/10.1016/j.copbio.2019.12.018
  18. 18. Minatel, I. O., Borges, C. V., Ferreira, M. I., Gomez, H. A. G., Chen, C. Y. O., & Lima, G. P. P. Phenolic compounds: Functional properties, impact of processing and bioavailability. In Soto-Hernández M, editor. Phenolic compounds—Biological activity. 1ra ed. IntechOpen; 2017. p. 1-24. http://dx.doi.org/10.5772/66368
  19. 19. Mecha, E., Leitão, S. T., Carbas, B., Serra, A. T., Moreira, P. M., Veloso, M. M., & Bronze, M. R. Characterization of soaking process’ impact in common beans phenolic composition: Contribute from the unexplored Portuguese germplasm. Foods. 2019; 8 (8): 296. https://doi.org/10.3390/foods8080296
  20. 20. Domínguez-Arispuro, D. M., Cuevas-Rodríguez, E. O., Milán-Carrillo, J., León-López, L., Gutiérrez-Dorado, R., & Reyes-Moreno, C. Optimal germination condition impacts on the antioxidant activity and phenolic acids profile in pigmented desi chickpea (Cicer arietinum L.) seeds. J. Food Sci. Technol. 2018; 55 (2): 638-647. https://doi.org/10.1007/s13197-017-2973-1
  21. 21. Monk, J. M., Wu, W., Hutchinson, A. L., Pauls, P., Robinson, L. E., & Power, K. A. Navy and black bean supplementation attenuates colitis-associated inflammation and colonic epithelial damage. J. Nutr. Biochem. 2018; 56: 215-223. https://doi.org/10.1016/j.jnutbio.2018.02.013
  22. 22. Aranda-Olmedo, I., & Rubio, L. A. Dietary legumes, intestinal microbiota, inflammation and colorectal cancer. J. Funct. Foods. 2020; 64: 103707. https://doi.org/10.1016/j.jff.2019.103707
  23. 23. Juárez-Chairez, M. F., Cid-Gallegos, M. S., Meza-Márquez, O. G., & Jiménez-Martínez C. Biological activities of chickpea in human health (Cicer arietinum L.). A review. Plant Foods Hum Nutr. 2020; 75 (2): 142-153. https://doi.org/10.1007/s11130-020-00814-2
  24. 24. Neri-Numa, I. A., Cazarin, C. B. B., Ruiz, A. L. T. G., Paulino, B. N., Molina, G., & Pastore, G. M. Targeting flavonoids on modulation of metabolic syndrome. J. Funct. Foods. 2020; 73: 104132. https://doi.org/10.1016/j.jff.2020.104132
  25. 25. Khan, M. I., Khan, S. M., Hussain, I., ur Rehman, S., Shah, S. H. R., Ayub, Q ., & ul Haq, N. Qualitative analysis of pea (Pisum sativum) seeds procured from different sources and locations of district Haripur-Khyber Pukhtunkhwa Pakistan. PAB. 2019; 8 (2): 1782-1788. http://dx.doi.org/10.19045/bspab.2019.80121
  26. 26. Bitocchi, E., Rau, D., Bellucci, E., Rodriguez, M., Murgia, M. L., Gioia, T., & Papa, R. Beans (Phaseolus ssp.) as a model for understanding crop evolution. Front. Plant Sci. 2017; 8: 722. https://doi.org/10.3389/fpls.2017.00722
  27. 27. Capistrán-Carabarin, A., Aquino-Bolaños, E. N., García-Díaz, Y. D., Chávez-Servia, J. L., Vera-Guzmán, A. M., & Carrillo-Rodríguez, J. C. Complementarity in phenolic compounds and the antioxidant activities of Phaseolus coccineus L. and P. vulgaris L. Landraces. Foods. 2019; 8 (8): 295. DOI: 10.3390/foods8080295
  28. 28. Dias, R., Oliveira, H., Fernandes, I., Simal-Gandara, J., & Perez-Gregorio, R. Recent advances in extracting phenolic compounds from food and their use in disease prevention and as cosmetics. Crit. Rev. Food Sci. Nutr. 2020; 1-22. https://doi.org/10.1080/10408398.2020.1754162
  29. 29. Peanparkdee, M., & Iwamoto, S. Encapsulation for improving in vitro gastrointestinal digestion of plant polyphenols and their applications in food products. Food Rev. Int, 2020; 1-19. https://doi.org/10.1080/87559129.2020.1733595
  30. 30. Lafarga, T., Villaró, S., Bobo, G., Simó, J., & Aguiló-Aguayo, I. Bioaccessibility and antioxidant activity of phenolic compounds in cooked pulses. Int. J. Food Sci. Technol. 2019; 54 (5): 1816-1823. DOI:10.1111/ijfs.14082
  31. 31. Gupta, R. K., Gupta, K., Sharma, A., Das, M., Ansari, I. A., & Dwivedi, P. D. Health risks and benefits of chickpea (Cicer arietinum) consumption. J. Agric. Food Chem. 2019; 65 (1): 6-22. https://doi.org/10.1021/acs.jafc.6b02629
  32. 32. Fan, G., & Beta, T. Discrimination of geographical origin of Napirira bean (Phaseolus vulgaris L.) based on phenolic profiles and antioxidant activity. J. Food Compos. Anal. 2017; 62: 217-222. https://doi.org/10.1016/j.jfca.2017.07.001
  33. 33. El-Feky, A. M., Elbatanony, M. M., & Mounier, M. M. Anti-cancer potential of the lipoidal and flavonoidal compounds from Pisum sativum and Vicia faba peels. Egypt. J. Basic Appl. Sci. 2018; 5 (4): 258-264. https://doi.org/10.1016/j.ejbas.2018.11.001
  34. 34. Giusti, F., Capuano, E., Sagratini, G., & Pellegrini, N. A comprehensive investigation of the behaviour of phenolic compounds in legumes during domestic cooking and in vitro digestion. Food Chem. 2019; 285: 458-467. https://doi.org/10.1016/j.foodchem.2019.01.148
  35. 35. Stanisavljević, N. S., Ilić, M. D., Matić, I. Z., Jovanović, Ž. S., Čupić, T., Dabić, D. Č., Natić, M. M., & Tešić, Ž. L. Identification of phenolic compounds from seed coats of differently colored European varieties of pea (Pisum sativum L.) and characterization of their antioxidant and in vitro anticancer activities. Nutr. Cancer. 2016; 68 (6):988-1000. https://doi.org/10.1080/01635581.2016.1190019
  36. 36. Telles, A. C., Kupski, L., & Furlong, E. B. Phenolic compound in beans as protection against mycotoxins. Food Chem. 2017; 214: 293-299. https://doi.org/10.1016/j.foodchem.2016.07.079
  37. 37. Yang, Q . Q ., Gan, R. Y., Ge, Y. Y., Zhang, D., & Corke, H. Ultrasonic treatment increases extraction rate of common bean (Phaseolus vulgaris L.) antioxidants. Antioxidants, 2019; 8 (4): 83. https://doi.org/10.3390/antiox8040083
  38. 38. Mojica, L., Meyer, A., Berhow, M. A., & de Mejía, E. G. Bean cultivars (Phaseolus vulgaris L.) have similar high antioxidant capacity, in vitro inhibition of α-amylase and α-glucosidase while diverse phenolic composition and concentration. Food Res. Int. 2015; 69: 38-48. https://doi.org/10.1016/j.foodres.2014.12.007
  39. 39. Brigide, P., Canniatti-Brazaca, S., Pereira, M. & Huber, K. Effect of cooking in common bean cultivars on antioxidant activity and phenolic compounds. Braz. J. Food Res. 2018; 9 (3): 1-7. DOI:10.3895/rebrapa.v9n3.4538
  40. 40. Eshraq, B., Mona, A., Sayed, A., & Emam, A. Effect of soaking, cooking and germination on chemical constituents and bioactive compounds as well as their cytotoxic activities of black bean extracts. Nat. Prod. Chem. Res. 2016; 4. 1-7. DOI:10.4172/2329-6836.1000237
  41. 41. Zilani, M. N. H., Sultana, T., Rahman, S. A., Anisuzzman, M., Islam, M. A., Shilpi, J. A., & Hossain, M. G. Chemical composition and pharmacological activities of Pisum sativum. BMC Complement Altern Med. 2017; 17 (1): 1-9. https://doi.org/10.1186/s12906-017-1699-y
  42. 42. Lomas-Soria, C., Pérez-Ramírez, I. F., Caballero-Pérez, J., Guevara-Gonzalez, R. G., Guevara-Olvera, L., Loarca-Piña, G., & Reynoso-Camacho, R. Cooked common beans (Phaseolus vulgaris L.) modulate renal genes in streptozotocin-induced diabetic rats. J. Nutr. Biochem. 2015; 26 (7): 761-768. https://doi.org/10.1016/j.jnutbio.2015.02.006
  43. 43. Ombra, M. N., d’Acierno, A., Nazzaro, F., Riccardi, R., Spigno, P., Zaccardelli, M., & Fratianni, F. Phenolic composition and antioxidant and antiproliferative activities of the extracts of twelve common bean (Phaseolus vulgaris L.) endemic ecotypes of southern Italy before and after cooking. Oxid. Med. Cell. Longev. 2016; 1-12. https://doi.org/10.1155/2016/1398298
  44. 44. Teixeira-Guedes, C. I., Oppolzer, D., Barros, A. I., & Pereira-Wilson, C. Impact of cooking method on phenolic composition and antioxidant potential of four varieties of Phaseolus vulgaris L. and Glycine max L. LWT-Food Sci Technol. 2019; 103: 238-246. https://doi.org/10.1016/j.lwt.2019.01.010
  45. 45. Maharjan, P., Penny, J., Partington, D. L., & Panozzo, J. F. Genotype and environment effects on the chemical composition and rheological properties of field peas. J. Sci. Food Agric. 2019; 99 (12): 5409-5416. https://doi.org/10.1002/jsfa.9801
  46. 46. Madrera, R. R., & Valles, B. S. Development and validation of ultrasound assisted extraction (UAE) and HPLC-DAD method for determination of polyphenols in dry beans (Phaseolus vulgaris). J. Food Compos. Anal. 2020; 85. https://doi.org/10.1016/j.jfca.2019.103334
  47. 47. Megías, C., Cortés-Giraldo, I., Alaiz, M., Vioque, J., & Girón-Calle, J. Isoflavones in chickpea (Cicer arietinum) protein concentrates. J. Funct. Foods. 2016; 21: 186-192. https://doi.org/10.1016/j.jff.2015.12.012
  48. 48. Gao, Y., Yao, Y., Zhu, Y., & Ren, G. Isoflavone content and composition in chickpea (Cicer arietinum L.) sprouts germinated under different conditions. J. Agric. Food Chem. 2015; 63 (10): 2701-2707. https://doi.org/10.1021/jf5057524
  49. 49. Monk, J. M., Wu, W., McGillis, L. H., Wellings, H. R., Hutchinson, A. L., Liddle, D. M., & Power, K. A. Chickpea supplementation prior to colitis onset reduces inflammation in dextran sodium sulfate-treated C57Bl/6 male mice. Appl. Physiol. Nutr. Metab. 2018; 43 (9): 893-901. https://doi.org/10.1139/apnm-2017-0689
  50. 50. Gan, Y., Fu, Y., Yang, L., Chen, J., Lei, H., & Liu, Q . Cyanidin-3-O-glucoside and cyanidin protect against intestinal barrier damage and 2, 4, 6-trinitrobenzenesulfonic acid-induced colitis. J. Med. Food. 2020; 23 (1): 90-99. https://doi.org/10.1089/jmf.2019.4524
  51. 51. Dueñas, M., Sarmento, T., Aguilera, Y., Benitez, V., Mollá, E., Esteban, R. M., & Martín-Cabrejas, M. A. Impact of cooking and germination on phenolic composition and dietary fibre fractions in dark beans (Phaseolus vulgaris L.) and lentils (Lens culinaris L.). LWT-Food Sci Technol. 2016; 66: 72-78. https://doi.org/10.1016/j.lwt.2015.10.025
  52. 52. López-Martínez, L. X., Leyva-López, N., Gutiérrez-Grijalva, E. P., & Heredia, J. B. Effect of cooking and germination on bioactive compounds in pulses and their health benefits. J. Funct. Foods. 2017; 38: 624-634. http://dx.doi.org/10.1016/j.jff.2017.03.002
  53. 53. Bulbula, D. D., & Urga, K. Study on the effect of traditional processing methods on nutritional composition and anti nutritional factors in chickpea (Cicer arietinum). Cogent Food Agric. 2018; 4 (1): 1422370. https://doi.org/10.1080/23311932.2017.1422370
  54. 54. Cárdenas-Castro, A. P., Pérez-Jiménez, J., Bello-Pérez, L. A., Tovar, J., & Sáyago-Ayerdi, S. G. Bioaccessibility of phenolic compounds in common beans (Phaseolus vulgaris L.) after in vitro gastrointestinal digestion: A comparison of two cooking procedures. Cereal Chem. 2020; 97 (3). https://doi.org/10.1002/cche.10283
  55. 55. Arribas, C., Cabellos, B., Cuadrado, C., Guillamón, E., & Pedrosa, M. M. The effect of extrusion on the bioactive compounds and antioxidant capacity of novel gluten-free expanded products based on carob fruit, pea and rice blends. Innov. Food Sci. Emerg. Technol. 2019; 52: 100-107. https://doi.org/10.1016/j.ifset.2018.12.003
  56. 56. Gu, B. J., Masli, M. D. P., & Ganjyal, G. M. Whole faba bean flour exhibits unique expansion characteristics relative to the whole flours of lima, pinto, and red kidney beans during extrusion. J. Food Sci. 2020; 85 (2): 404-413. https://doi.org/10.1111/1750-3841.14951
  57. 57. Ferreira, C. D., Bubolz, V. K., da Silva, J., Dittgen, C. L., Ziegler, V., de Oliveira Raphaelli, C., & de Oliveira, M. Changes in the chemical composition and bioactive compounds of chickpea (Cicer arietinum L.) fortified by germination. LWT-Food Sci Technol. 2019; 111: 363-369. https://doi.org/10.1016/j.lwt.2019.05.049
  58. 58. Xu, M., Jin, Z., Ohm, J. B., Schwarz, P., Rao, J., & Chen, B. Effect of germination time on antioxidative activity and composition of yellow pea soluble free and polar soluble bound phenolic compounds. Food Funct. 2019; 10 (10): 6840-6850. DOI: 10.1039/C9FO00799G
  59. 59. Worku, A., & Sahu, O. Significance of fermentation process on biochemical properties of Phaseolus vulgaris (red beans). Biotechnol. Rep. 2017; 16: 5-11. https://doi.org/10.1016/j.btre.2017.09.001
  60. 60. Uzeta, C. M., Cuevas-Rodriguez, E. O., Cervantes, J. L., Carrillo, J. M., Dorado, R. G., & Moreno, C. R. Improvement nutritional/antioxidant properties of underutilized legume tepary bean (Phaseolus acutifolius) by solid state fermentation. Agrociencia, 2019; 53 (7): 987-1003
  61. 61. Fan, Y., & Pedersen, O. Gut microbiota in human metabolic health and disease. Nat. Rev. Microbiol. 2020; 1-17. https://doi.org/10.1038/s41579-020-0433-9
  62. 62. Forgie, A. J., Gao, Y., Ju, T., Pepin, D. M., Yang, K., Gänzle, M. G., Ozga, J. A., Chan, C. B., & Willing, B. P. Pea polyphenolics and hydrolysis processing alter microbial community structure and early pathogen colonization in mice. J. Nutr. Biochem. 2019; 67: 101-110. https://doi.org/10.1016/j.jnutbio.2019.01.012
  63. 63. Coman, V., & Vodnar, D. C. Hydroxycinnamic acids and human health: Recent advances. J. Sci. Food Agric. 2020; 100 (2): 483-499. https://doi.org/10.1002/jsfa.10010
  64. 64. Liu, P., Bian, Y., Fan, Y., Zhong, J., & Liu, Z. Protective effect of naringin on in vitro gut-vascular barrier disruption of intestinal microvascular endothelial cells induced by TNF-α. J. Agric. Food Chem. 2020; 68 (1): 168-175. https://doi.org/10.1021/acs.jafc.9b06347
  65. 65. Sánchez Chino, X. M., Jiménez Martínez, C., Vásquez Garzón, V.R., Álvarez González, I., Villa Treviño, S., Madrigal Bujaidar, E., Dávila Ortiz, G., & Baltiérrez Hoyos R. Cooked chickpea consumption inhibits colon carcinogenesis in mice induced with azoxymethane and dextran sulfate sodium. J. Am. Coll. Nutr. 2017; 36 (5): 391-398. https://doi.org/10.1080/07315724.2017.1297744
  66. 66. Chen, P. X., Zhang, H., Marcone, M. F., Pauls, K. P., Liu, R., Tang, Y., Zhang, B., Renaud, J. B., & Tsao, R. Anti-inflammatory effects of phenolic-rich cranberry bean (Phaseolus vulgaris L.) extracts and enhanced cellular antioxidant enzyme activities in Caco-2 cells. J. Funct. Foods. 2017; 38: 675-685. https://doi.org/10.1016/j.jff.2016.12.027
  67. 67. Chen, G., Wang, G., Zhu, C., Jiang, X., Sun, J., Tian, L., & Bai, W. Effects of cyanidin-3-O-glucoside on 3-chloro-1, 2-propanediol induced intestinal microbiota dysbiosis in rats. Food Chem. Toxicol. 2019; 133: 110767. https://doi.org/10.1016/j.fct.2019.110767
  68. 68. Luzardo-Ocampo, I., Campos-Vega, R., Gaytán-Martínez, M., Preciado-Ortiz, R., Mendoza, S., & Loarca-Piña, G. Bioaccessibility and antioxidant activity of free phenolic compounds and oligosaccharides from corn (Zea mays L.) and common bean (Phaseolus vulgaris L.) chips during in vitro gastrointestinal digestion and simulated colonic fermentation. Food Res. Int. 2017; 100: 304-311. https://doi.org/10.1016/j.foodres.2017.07.018
  69. 69. Edwards, C. A., Havlik, J., Cong, W., Mullen, W., Preston, T., Morrison, D. J., & Combet, E. Polyphenols and health: Interactions between fibre, plant polyphenols and the gut microbiota. Nutr. Bull. 2017; 42 (4): 356-360. https://doi.org/10.1111/nbu.12296
  70. 70. Cirkovic Velickovic, T. D., & Stanic-Vucinic, D. J. The role of dietary phenolic compounds in protein digestion and processing technologies to improve their antinutritive properties. Compr. Rev. Food Sci. Food Saf. 2018; 17 (1): 82-103. https://doi.org/10.1111/1541-4337.12320

Written By

Mayra Nicolás-García, Cristian Jiménez-Martínez, Madeleine Perucini-Avendaño, Brenda Hildeliza Camacho-Díaz, Antonio Ruperto Jiménez-Aparicio and Gloria Dávila-Ortiz

Submitted: 06 April 2021 Reviewed: 30 April 2021 Published: 29 June 2021