Antioxidants, Vol. 12, Pages 48: Anthocyanins: Metabolic Digestion, Bioavailability, Therapeutic Effects, Current Pharmaceutical/Industrial Use, and Innovation Potential

4.1. Anthocyanins As Natural Dyes in the Food IndustryColor is an important feature of foods that remarkably affects consumer perception of the product’s overall quality attributes. The food industry mainly uses synthetic colorants to improve the color appearance of formalized food products. Conversely, the popularity of anthocyanins is rising as natural coloring agents in the food industry. Until now, more than 600 anthocyanin derivatives have been reported, and they are known as non-toxic and water-soluble compounds, which lead to sufficient dying of food systems [112]. Therefore, anthocyanins are considered one of the most important natural food colorants which are incidentally allowed for use as food dyes by EFSA with the code of E163 given its attractive colors ranging from red to blue [113].Artificial food colorants are, however, the main and preferred source of colorants due to their higher processing and storage stability, effective coloring, and low cost [114]. However, consumer consciousness toward natural products have forced the food industry to rethink the use of synthetic food additives due in large part to consumer concerns regarding the possible health side effects of synthetic colorants, resulting in the prohibition of some of them [115]. As such, food scientists are focusing on optimizing crop extraction conditions, purification, processing cost, and the color stability of natural food colorants [113,116,117,118]. The color of the medium, including anthocyanins, alters depending on the pH value of the medium. The red flavylium cations of anthocyanins are present in highly acidic medium (pH ≤ 3), while a higher pH value causes lower color intensity due to decreased concentration of the flavylium cation, which results in the formation of colorless carbinol pseudobase by the nucleophilic attack of the water. Finally, if the medium pH alters from low acid to basic conditions (5 ≤ pH ≤ 8), the violet/blue quinonoidal forms occur due to deprotonation of the flavylium cation [119]. This means pH is the most critical physiochemical factor in obtaining a desirable medium color.Research studies indicate that plant-based anthocyanins are successful in coloring various food mediums such as bakery products, dairy products, powder, mixes, juices, candies, alcoholic beverages, jams, confectionery products, and ice cream [114,116,117,120,121,122]. Some of the research studies associated the coloring of the foodstuffs by the addition of anthocyanins, and are summarized in Table 3.The extraction of anthocyanins from natural sources is not easy due to the quick decomposition of these compounds under pH alteration, high temperature, and the presence of light, ascorbic acid, and oxygen [123]. As such, the application of anthocyanins within the food industry as a colorant is still limited because of feasibility, stability, and high-cost concerns. To eliminate these concerns and obtain an anthocyanin-rich extract or a powder with the highest quality, novel approaches in the extraction of anthocyanin compounds are emerging, such as ultrasound-assisted extraction, high pressure-assisted extraction, pulsed electric field-assisted extraction, microwave-assisted extraction, and enzyme-assisted extraction. Additionally, anthocyanin compounds can be extracted from plant sources by thermal and non-thermal alone, or by combining these technologies [115,124,125]. 4.2. Applications of Anthocyanins as Prebiotics IngredientsFoods have a significant role in impacting gut microbiota, influencing its composition in abundance and diversity. Dietary habits can profoundly impact the composition of gut microbiota, affecting individuals’ health [124]. This could be modulated by using prebiotics, which is a beneficial element to stimulate the growth and activity of favorable bacteria in the human digestive system, particularly in the large intestine, to preserve a healthy body.Prebiotics can be found in various food sources such as bananas, red onion, garlic, asparagus, barley, and nuts, among others [125]. It is recognized that anthocyanins are a potential prebiotic source, given that they can enhance the growth of probiotic bacteria and hinder the growth of pathogenic bacteria [126]. Anthocyanins and prebiotics affect wellness and overall health, possibly through the modulation of the microbiota and the intestinal ecosystem [127].Clinical and in vitro experiments have shown the favorable characteristics of anthocyanins on microbiota [128,129,130]. Recent evidence suggests that when they are consumed, anthocyanins can be found to present all the way through the length of the gastrointestinal tract (colon included), where gut microbiota is likely to have a critical role in their bioactivity. Similarly, anthocyanins may positively influence microbiota balance [65,131,132]. Research indicates that the upper digestive tract does not readily absorb anthocyanin, and most of it reaches the large intestinal tract [133].Black soybean (Glycine max (L.) Merr.) is a nutritionally rich food with a considerable supply of calories and protein and also contains carotenoids, isoflavones, saponins, vitamin E, and anthocyanins, which have been described as being able to exert biological activity [134]. Several considerable health-related effects were described for black beans, such as their ability to reduce the frequency of DNA damage by cyclophosphamide [131] and reduce low-density lipoprotein oxidation [132]. However, research on the anthocyanin prebiotic potential of Indonesian black soybean is very limited. Pramitasari and colleagues compared the prebiotic activity from an extract, whole black soybean flour, and the extract residue of the Indonesian black soybean, and their data revealed that the greatest value of prebiotic activity was attained from anthocyanin extract, then the whole black soybean flour, and finally the anthocyanin extract residue [126]. This team’s in vitro studies used Lactobacillus acidophilus as the probiotic bacteria, while Escherichia coli and Salmonella typhi were employed as the pathogenic bacteria. The authors of this research concluded that anthocyanins demonstrate possibilities as a prebiotic source given their role in stimulating the growth of probiotic bacteria and in pathogenic bacteria inhibition. The Indonesian black soybean showed promise as a prebiotic source, given its elevated anthocyanin content [126]. Consequently, more research on the specific mechanisms of how anthocyanins from black soybeans might stimulate probiotic bacteria growth while simultaneously inhibiting pathogenic bacteria is necessary. Additionally, in this light, further studies are still necessary to explore the prebiotic activity using in vivo tests to expose its potential efficacy on human health [126].Anthocyanins derived from certain berries, such as cranberry, bilberry, and blueberry, might inhibit E. coli and S. Typhi growth due to morphological damage, changes to the structure, destruction of cell wall structures, membranes, and the intracellular matrix of pathogenic bacteria. Anthocyanins may also hinder the activity of enzymes by executing oxidation reactions in the sulfhydryl group or non-specific interactions with protein components, which lead to the inactivation and functional losses of the enzymes produced by pathogenic bacteria necessary for their survival. Anthocyanins’ antimicrobial activities can happen because of several processes and the combined effects of various phytochemical components in anthocyanins, such as phenolic and organic acids [135,136]. In research conducted by Fotschki and colleagues, it was demonstrated that anthocyanins found in strawberries might play a beneficial role in the development of probiotic bacteria [137]. These probiotic bacteria could metabolize anthocyanins in the human intestine and improve short-chain fatty acid production. These molecules were judged to have a beneficial effect on the large intestine due to probiotic bacteria growth stimulation as well as the demonstrated antimicrobial activity against enteropathogenic bacteria. Zhang and colleagues reported that bifidobacteria supplemented with the anthocyanins from purple sweet potatoes (Solanum tuberosum) produced a large amount of phenolic/organic acids during the cultivation period, indicating that the anthocyanins could be utilized as prebiotics, not to mention that a low concentration of anthocyanins (bifidobacteria and may thus serve as a prebiotic [138].The comparative population of two bacteria groups prevalent in the gut, Bacteroidetes, and Firmicutes, can be associated with a high-fat diet, overnutrition, and obesity, with Bacteroidetes, decreasing and Firmicutes increasing with these conditions [139,140]. The ratio of Bacteroidetes is lowered in obese people compared with lean people, and the proportion of Bacteroidetes increases with weight loss [141]. The increased ratio of Firmicutes: Bacteroidetes denotes a dysbiotic environment exemplified by escalated systemic and gastrointestinal tract inflammation which has undesirable outcomes [124,142]. Obesity affects the nature of intestinal microbiota, and these differences can affect the efficiency of caloric extraction from food [143]. A recent open-label study in modulating intestinal microbiota and intestinal inflammation used 51 male and female volunteers (between the ages of 18 and 50) with uncomplicated obesity (body mass index (BMI) of 29.9 − 39.9 ± 1 kg/m2), where they were given daily supplementation of anthocyanin and prebiotic blend for eight weeks. This supplementation was in the form of a powder sachet, and every morning one sachet was taken with breakfast by mixing into a beverage or food of choice. The supplement delivered 215 mg anthocyanins (144 mg European blueberry extract (35 mg anthocyanins), 202 mg black currant extract (60 mg anthocyanins), and 618 mg black rice extract (120 mg anthocyanins) and 2.7 g prebiotic fibers (1.9 g inulin and 1.1 g fructooligosaccharides)) daily. At the end of the study, the participants’ weight did not change substantially, with 94.8 ± 13.1 kg at baseline, 95.1 ± 13.0 kg at four weeks, and 94.9 ± 12.8 kg at eight weeks, respectively. Additionally, the BMI did not change meaningfully during the study, with a BMI of 34.0 ± 3.1 kg/m2 at baseline, 34.1 ± 3.1 kg/m2 at four weeks, and 34.0 ± 3.2 kg/m2 at eight weeks. After eight weeks of supplementation, participants presented a statistically significant increase in Bacteroidetes (from 13.8% to 34.5%) and a statistically significant decline in Firmicutes:Bacteroidetes ratio (from 14.2 to 9.3), Firmicutes (from 74.9% to 59%), and Actinobacteria (from 8.5% to 3.4%). These three phyla comprised 97.2% of the bacterial composition at baseline and 96.9% following 8-week supplementation. The supplementation was revealed to be safe and suggested that the routine use of the anthocyanin-prebiotic blend modulated the intestinal ecosystem positively. Bowel habits were made better as demonstrated by decreases in the severity of gas, bloating, and abdominal pain, not to mention considerable improvements in stool consistency. The hemoglobin A1c (HbA1c), a marker of long-term glucose regulation, had a statistically significant decrease from 5.51 ± 0.37 mmol/L to 5.35 ± 0.39 mmol/L at baseline and the end of the study, respectively. Additionally, four participants with heightened HbA1c were prediabetic, and one was diabetic at the beginning of the study. However, following supplementation, these participants showed a reduction or normalization in HbA1c levels (Hester et al., 2018). More studies have suggested that anthocyanins have an anti-obesity effect that may be connected to their microbiota modulation [32]. These anti-obesity effects physiologically include the prevention of inflammation, body fat accumulation, dyslipidemia, and insulin resistance [144]. A more extended study to examine weight loss is necessary to verify if a lower Firmicutes:Bacteroidetes ratio might decrease weight, given that Firmicutes are more efficient in extracting energy from foods than Bacteroidetes [145,146]. Further research is required to establish whether an anthocyanin-prebiotic blend might impact weight control, especially since previous research demonstrates anthocyanin’s anti-obesity benefits for obese populations through gut microbiota interactions [147].Irritable bowel syndrome (IBS) is a widespread form of functional disorder characterized by abdominal discomfort and pain related to altered bowel function [148,149], a syndrome that is still lacking effective prevention therapies. Very limited research exists that examines the impacts of prebiotics in modulating gut microbiota for inhibiting IBS development [150]. However, research using in vivo and in vitro models aims to establish a novel prebiotic blend (PB) composed of fructo-oligosaccharide, galactooligosaccharide, inulin, and anthocyanins, which could help inhibit the development of IBS. To ascertain whether PB improved inflammatory status on a mice model and Salmonella stimulated Caco-2 cells, the data showed the manifestation of pro-inflammatory mediators in colon tissues and Caco-2 cells. Within these Caco-2 cells, the activation of TNF-α, IL-1B, and IL-8 induced by S. typhimurium could be hindered by PB. Both in vitro and in vivo results suggested that PB could attenuate inflammation in the Caco-2 cells and the IBS mice model. Pre-treatment with a prebiotic blend in mice considerably lowered the gravity of IBS symptoms, which offers biological credibility for the suitability of this prebiotic product. PPAR signaling has a direct link with the anti-inflammatory impacts of PB (PPARγ signaling changed significantly (p150].Bilberry was studied as a source of anthocyanins, and the results revealed that a medium dose of anthocyanin extract for consumption was 20 mg/kg bw/day. It was the most advantageous quantity for controlling the intestinal function of aging rats [151]. The Firmicutes:Bacteroidetes proportion grew (2.83 to 2.99) with the age progression of rats. The major phylum began to shift from Firmicutes in the direction of Bacteroidetes 53.18% before medium-dose bilberry anthocyanin (MBA) extract consumption vs. 58.18% after MBA ingestion (17.81% vs. 29.25%, respectively). Additionally, there were considerable reductions in the comparative abundance of Verrucomicrobia (from 0.0236 to 0.0016), and Euryarchaeota (from 0.1162 to 0.0325) found after MBA intake. After MBA ingestion, considerable enhancements to the comparative abundance of Lactobacillus and Bacteroides and a decline in Methanobrevibacter. Microbial activity modulation was suggested through statistically significant variations in the digestive enzymes’ actions in the cecal contents. The intake of berry anthocyanin extract (BA) in a diet significantly diminished the activities of the digestive enzymes β-glucuronidase, α, and β-glucosidase, and α and β-galactosidase in the cecum [151].Berry anthocyanin extract consumption could reestablish inflammatory factors to normal levels by diminishing D-LA and LPS levels. These actions were reliable with changes in the cecal contents with respect to starch-utilizing bacteria (Aspergillus oryzae) and short-chain fatty acids (SCFAs). BA promoted the generation of SCFAs (acetic, propionic, and butyric acids) by controlling intestinal microbial flora. The SCFAs not only served as energy sources for intestinal mucosa, but also performed a crucial part in maintaining the integrity of the intestinal barrier. Bioantagonism occurs between gut microbiota, and the normal gut microbiota forms an intestinal mucosal barrier through adhering, colonizing, and multiplying. Through antagonism, BA repulses intestinal mucosal invasions by harmful bacteria to achieve a complex and dynamic equilibrium between the body and the gut microbiota, thus performing an anti-aging intervention [151]. Following the consumption of BA, bacteria beneficial to the intestine (Bacteroides, Aspergillus oryzae, Clostridiaceae-1, Lactobacillus, the Bacteroidales-S24-7-group, and the Lachnospiraceae-NK4A136-group) were stimulated to grow, and hurtful bacteria (Euryarchaeota and Verrucomicrobia) were suppressed, which promoted acetic, butyric, and propionic acid content. Nevertheless, the ingestion of a high dose of bilberry anthocyanin extract (40 mg/kg bodt weight/day) altered some intestinally beneficial bacteria in an undesirable way [151]. The authors of this work, exploring the bilberry anthocyanin extract action on intestinal barrier function and gut microbiota, which used aging rats, concluded that consuming a bilberry anthocyanin extract, taking into consideration the effective dose, is a thinkable method for assisting healthy people aging [151].Research on comicroencapsulation by freeze-drying the anthocyanins from an aqueous extract of black beans and Lactobacillus casei into a novel blend of whey protein isolate (WPI), chitosan, and inulin, intended to amplify the efficiency of encapsulated anthocyanins, and the survivability of bacteria in a gastrointestinal juice simulation, was performed. The encapsulation efficiency (EE) was 77.42 ± 1.34% for Lactobacillus casei and 99.33 ± 0.13% for anthocyanins [152]. Comicroencapsulation of prebiotics and probiotics demonstrated additional survivability because of their synergistic relationship [153]. Comicroencapsulation increased the potential to provide better bioactivity of coencapsulated ingredients [154].In vitro digestibility results validated the encapsulants’ shielding effect in a gastric environment and a regulated delivery within intestinal conditions [155]. The phytochemical profile in comicroencapsulated powder underscored the presence of 1.65 ± 0.13 mg cyanidin-3-glucoside (C3G) equivalents per g dry weight of powder (mg/g DW), phenolic compounds of 21.64 ± 0.98 mg gallic acid equivalent (GAE)/g DW, flavonoids of 3.71 ± 0.10 mg catechin equivalents (CE)/g DW, yielding an antioxidant activity of 157.22 ± 4.13 mMol Trolox/g DW. The repressive action of the comicroencapsulated powder towards α-glucosidase and α-amylase was elevated by approximately 39% and 68%, respectively. These values correspond to IC50 of 278.72 ± 12.34-μg GAE/mL and 160.35 ± 1.25 μg GAE/mL, respectively. These findings indicate that comicroencapsulated powder may well be capable of reducing glucose uptake/absorption. The powder was incorporated as a natural ingredient into a food matrix (soft cheese), and no substantial variations were discovered in the phytochemical profile of the samples. In contrast, an upsurge of 0.5 log in colony-forming units (CFU)/g DW was discovered in value-added foods when contrasted with control, signifying a microcapsule bacterial release [152]. Vasile and colleagues suggest that the obtained powder might be promising for natural pigments, substituting synthetic colorants ordinarily used in the food industry, and playing a role in the possible health benefits linked to anthocyanins and lactic bacteria consumption [152].An analogous study applied comicroencapsulation (co-ME) to anthocyanins taken from cornelian cherry fruits and bacterial lactic acid through freeze-drying [155]. Because of the lacking stability of anthocyanins in minor alkaline conditions, like those typically found in the intestinal tract, anthocyanin bioavailability may be diminished. Microencapsulation (ME) is possibly one of the most researched and employed technologies for shielding bioactives from degradation. Regarding food and pharmaceutical uses, wall materials include natural biopolymers such as starches, proteins from dairy products, and natural gums, all of which are food compatible and safe. This technology was employed to find a useful food ingredient through the co-ME of the aqueous extract of cornelian cherry fruit with Lactobacillus casei through freeze-drying. The ME materials were selected as WPI, chitosan, and inulin. The five phenolic compounds identified were: cyanidin-3-rutinoside (72.77%), cyanidin-3-glucoside (5.42%), pelargonidin-3-glucoside (3.05%), pelargonidin-3-rutinoside (2.42%), and delphinidin-3-galactoside (1.03%). The contents of delphinidin-3-galactoside, pelargonidin-3-glucoside, and pelargonidin-3-rutinoside were, respectively, 4.31 mg/100 g DW, 12.73 mg/100 g DW, and 9.12 mg/100 g DW. The EE achieved in this investigation for anthocyanins was 89.16 ± 1.23% and 80.33 ± 0.44% for lactic acid bacteria. To determine the bioactives’ and lactic acid bacteria’ stability from the powder, the EE was established after storing in the dark at 4 °C for three months. The EE was 87.00 ± 1.56% for anthocyanins and 74.79 ± 0.71% for lactic acid bacteria. The freeze-drying technique permitted the researchers in this study to obtain a red-pink powder with a substantial amount of bioactive phenolic compounds and viable cells of 9.39·× 109 CFU/g DW.Regarding the total phytochemical profile of the co-ME powder, the extract demonstrated a total anthocyanins content (TAC) of 19.86 ± 1.18 mg C3G/g DW and total phenolic compound content (TPC) of 7.88 ± 0.22 mg GAE/g DW, producing an antioxidant action of 54.43 ± 0.73 mg Trolox/g DW. In vitro digestibility of the anthocyanins exhibited a substantial discharge of anthocyanins, and it was examined in the gastric phase, with a limit of 50% after digesting for 60 min. The anthocyanins declined considerably in simulated intestinal juice, with a max of approximately 37% after 120 min of digestion. The powder showed a smaller repressive effect in contrast to α-glucosidase of 24.13 ± 0.01% when contrasted with α-amylase, with a repressive impact of 89.72 ± 1.35%. The stability of lactic acid bacteria was determined after storing at 4 °C in the dark for three months. There was a minor discharge of anthocyanins from microcapsules with a rise of roughly 4% and a reduction of approximately 41% in TPC, with no substantial variations in antioxidant activity. The co-ME powder demonstrated a reduction in viable cells of L. casei431® after 90 days with only 0.47 log CFU/g DW. To find the volume of powder for food functionalization, various ratios of 2% (S1) and 5% (S2) were mixed with yogurt. The products were studied for their phytochemicals’ stability over a period of 21 days at 4–6 °C. In S1, after 21 days, a three-fold rise in TAC content was seen. For S2, an increase of 1.5-fold in TAC was observed, which suggested a liberation in anthocyanins from microparticles, while TPC was stable. Aside from substantial bioactive content, both S1 and S2 demonstrated improved antioxidant activity when contrasted with the control. It was, therefore, feasible to examine the value-added products that used the content of the cornelian cherry and lactic bacteria bioactive compounds in a stable, co-ME state, with the intention of creating health-supporting ingredients with various functions for food purposes. More research on the in vivo digestion of anthocyanins in distinct food matrices is necessary to establish the health effects of anthocyanin consumption [155]. The evidence shows the possibility of developing multi-functional ingredients from plant bioactive resources and lactic acid bacteria for uses such as nutraceuticals or food products. Further research is, however, required to clarify the efficiency of these powders for reported health effects and the mechanism of action in each case.Co-encapsulation can be a valuable technique for modifying the intestinal microbiota to achieve, restore, and maintain a positive balance in the gastrointestinal tract (GIT) ecosystem by introducing more resistant probiotic microorganisms. Numerous reports confirm the tolerance of the co-encapsulated probiotic live organisms to the stomach’s acidic environment in the presence of prebiotics. Future research should aim to increase the survival of probiotics in vivo, and more examples of the functional foods containing these ingredients need to be developed and tested [156].

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