Bioaccessibility of phenolic compounds from a wheat beer enriched with alginate-encapsulated wine industry by-product

Bioacessibilidade de compostos fenólicos de uma cerveja de trigo enriquecida com subproduto da indústria vinícola encapsulado em alginato

ABSTRACT:

Wine industry by-product (WIBP) encapsulated in alginate beads were incorporated to beer to increase antioxidant properties. The phenolic profile, in vitro bioaccessibility and gut metabolism were assessed. Scanning electron micrographs of the beads with WIBP revealed a relatively rough surface with large pores with craters, but without cracks, which ensures the protection of the encapsulated compounds. X-ray diffraction profiles showed the attenuated of the crystalline peaks, indicating the interactions between alginate and Ca²⁺. The WIPB antioxidant activity was assessed by FRAP (0.13 mmol Fe²⁺/g WIBP) and TEAC (0.078 mmol Trolox/g WIBP). The phenolic profile of the craft beer was not altered after the immersion of the beads for 60 days, maintaining its six free phenolic compounds (gallic, 3,4-dihydroxyphenylacetic, 4-hydroxybenzoic, 2,4-dihydroxybenzoic, ferulic, and salicylic acids). The phenolic compounds observed in WIBP and not in the craft beer (quercetin, rutin and syringic acids) were only detected after simulated digestion of WIBP beads that had been immersed in the beer, showing that the encapsulation of WIBP with calcium alginate beads protected the phenolic compounds until consumption. Total phenolic content increased after simulated digestion, and after gut fermentation. During this process the phenolic compounds diversity in each digestion step also increased. Therefore, the enrichment of beer with alginate beads containing the WIBP not only increases the content of phenolic compounds ingested by the consumer, but also the bioaccessibility of those compounds in relation to beer without the beads.

Key words:
Phenolic; beer; bioaccessibility; encapsulation; beads; wine industry by-product; antioxidant

RESUMO:

Subprodutos da indústria do vinho (WIBP, do inglês wine industry by-product) encapsulados em esferas de alginato foram incorporados à cerveja para aumentar as propriedades antioxidantes. O perfil fenólico, a bioacessibilidade in vitro e o metabolismo intestinal foram avaliados. As micrografias eletrônicas de varredura dos grânulos com WIBP revelaram uma superfície relativamente rugosa, com grandes poros com crateras, mas sem fissuras, o que garante a proteção dos compostos encapsulados. Os perfis de difração de raios-x mostraram atenuação dos picos cristalinos, indicando as interações entre alginato e Ca²⁺. A atividade antioxidante do WIPB foi avaliada por FRAP (0,13 mmol Fe²⁺/g WIBP) e TEAC (0,078 mmol Trolox/g WIBP). O perfil fenólico da cerveja artesanal não foi alterado após a imersão das esferas por 60 dias, mantendo seus seis compostos fenólicos livres (ácidos gálico, 3,4-dihidroxifenilacético, 4-hidroxibenzóico, 2,4-dihidroxibenzóico, ferúlico e salicílico). Os compostos fenólicos observados no WIBP e não na cerveja artesanal (quercetina, rutina e ácidos seríngicos) só foram detectados após digestão simulada de esferas de WIBP imersas na cerveja, mostrando que o encapsulamento de WIBP com esferas de alginato de cálcio protegeu os compostos fenólicos até o consumo. O conteúdo fenólico total aumentou após a digestão simulada e após a fermentação intestinal. Durante este processo a diversidade de compostos fenólicos em cada etapa da digestão também aumentou. Portanto, o enriquecimento da cerveja com esferas de alginato contendo o WIBP não só aumenta o teor de compostos fenólicos ingeridos pelo consumidor, mas também a bioacessibilidade desses compostos em relação à cerveja sem as esferas.

Palavras-chave:
Compostos fenólicos; cerveja; bioacessibilidade; encapsulamento; subproduto da indústria vinícola; antioxidante

INTRODUCTION

Wine industry has faced a huge problem for years: the disposal of the solid residue generated by winemaking activities, which includes grape pomace, lees, stalk and sludge (CONTRERAS et al., 2022). Grape pomace is the main solid by-product and is composed of seeds (38 - 52 %) and seedless pomace (48 - 62 %), consisting of stems, skins and residual pulp (BERES et al., 2017). Wine industry by-products, estimated in more than 11 million tonnes per year, are usually used as animal feed or as a vineyard fertilizer, but huge amounts are still wasted (CONTRERAS et al., 2022).

Grapes are recognized as a health promoting fruit, especially because of high amounts of bioactive compounds, such as polyphenols, including anthocyanins and tannins, vitamins, etc. Therefore, the interest on the valorization of the winery by-products has been growing based on their bioactive compounds (FERREYRA et al., 2023). Polyphenolic compounds are important phytochemicals, due to their multiple physiological properties, including antioxidant and antimicrobial activities (GARCÍA-RUIZ et al., 2009). Recently, we have optimized the encapsulation of a wine industry by-product (WIBP) by ionotropic gelation with sodium alginate with regards of beer incorporation, reducing erosion degree and swelling behavior of the beads (VIEIRA et al., 2019).

Beer is one of the most consumed alcoholic beverages in the world and its phenolic compounds, which arise from malt and hops, can be improved by technological strategies, contributing to flavor and color (CARVALHO & GUIDO, 2022). In comparison to wine, which is also a popular beverage, beer contains some polyphenol classes (chalcones and flavanones) that are not found in wine and wine contains others (stilbenes, proanthocyanidins) that are not found in beer. However, literature data reveals that wine is the beverage with a higher content of phenolic compounds and with higher antioxidant activity (RADONJIĆ et al., 2020). Although, synthetic antioxidants have been traditionally added to beer to increase stability, industries are reducing this approach because of consumers’ demands and firmer regulations (ZHAO et al., 2010). VELJOVIC et al. (2015) have shown that adding grapes to beer fermentation increased the phenolic content and antioxidant capacity of beers, indicating that grape-added beer is a better source of natural antioxidants than regular lager beer.

To enhance the retention time of phenolics in the intestinal tract and control its release in the body, encapsulation strategies have been proposed. Ionic gelation constitutes a simple, efficient, and low-cost encapsulation technique without the need for specialized equipment, high temperature, or organic solvents, making it appropriate for either hydrophobic or hydrophilic compounds (PEREIRA SILVEIRA et al., 2023). As an anionic polymer with carboxyl end groups, alginate is a good mucoadhesive agent. In gastric fluid (pH ± 1.2), the alginate hydrogel becomes a porous insoluble membrane that protects the encapsulated compounds, which turns into a soluble viscous film in the higher pH (pH ± 7.4) of the intestinal tract, resulting in the fast release of the encapsulated compounds (ZHAO et al., 2013). Bioaccessibility assays with encapsulated grape pomace extracts has shown a great potential of this technique for the release of phenolic compounds during gastrointestinal digestion (MARTINOVIĆ et al., 2023), but the capsules were not inserted in food products.

Therefore, the present study evaluated de addition of grape pomace residues from a wine industry (WIBP) encapsulated in alginate beads to a wheat beer to access the protective effect of the beads in relation to the phenolic content, and to investigate their bioaccessibilty and gut metabolism in a simulated digestion model.

MATERIALS AND METHODS

Materials

Sodium alginate was purchased from Sigma^®, with a mannuronic acid to guluronic acid residues ratio of 0.4 to 1.9. Calcium chloride was obtained from Vetec^®. The WIBP used for this study was the Alicante Bouschet grape pomace from red wine production, that was provided by Rio Sol Winery (Lagoa Grande, Pernambuco, Brazil). The pomace was dried at 60 °C in a tray dryer for 24 h and grinded in a Micro mill type Willye (Model: TE-648) with stainless steel screen with 20 mesh. The craft wheat beer used in the present work was purchased at a local marketplace located in Rio de Janeiro, Brazil. The following commercial standards of phenolic compounds were acquired from Sigma-Aldrich (St. Louis, MO): 2,4-dihydroxybenzoic, 3,4-dihydroxybenzoic, caffeic, gallic, ferulic, syringic, m-coumaric, 3,4-dihydroxyphenylacetic, p-coumaric, salicylic, and 4-hydroxybenzoic acids, quercetin acid, and rutin. Sodium carbonate was purchased from Spectrum Chemical Manufacturing Corp. (Gardena, CA).

Encapsulation process by ionotropic gelation

The general encapsulation process by inotropic gelation was performed as described by VIEIRA et al. (2019). Sodium alginate (1.5 % w/v) was dissolved in distilled water with WIBP (4 % w/v). The polymer solution was then added dropwise into the gelation media consisting of 250 mL of CaCl₂ solution (0.26 % w/v) using a 25 mL hypodermic syringe (without needle), under constant stirring at room temperature. The WIBP beads, once formed, were left in the gelation medium for 26 minutes (complexation time), collected by filtration, and washed with distilled water.

Morphological and physical characterization of beads

Prior to the analyses, WIBP beads were dried at 40 °C for 24 hours and ground in a ceramic mortar. Scanning electron microscopy: The morphology of the WIBP beads was observed in a scanning electron microscope (SEM) of Jeol brand, model JSM-6510LV. The dried beads were fixed to 10 mm diameter cylindrical metal supports using a double-sided carbon adhesive tape. The voltage acceleration used was 15 or 20 kV. X-ray Diffraction: X-ray diffraction (XRD) profiles of the dried WIBP beads, alginate and WIBP were obtained using a bench dust diffractometer (D2 Phaser-BRUKER) equipped with a linear detector (LYNXEYE), X-ray tube with anode (wavelength of 1.541 Å, voltage of 30 kV, current of 10 mA and maximum power of 300 W) and scanning with angular precision of ± 0.002° in the range of -2° to 150° in 2θ. Phase identification was performed using Diffrac software (Eva^TMof BRUKER).

Antioxidant activity

The antioxidant activity of the wheat beer and the WIBP were evaluated by the TEAC (Trolox Equivalent Antioxidant Capacity) and FRAP (Ferric Reducing Antioxidant Power) assays. For WIBP an extraction procedure was performed as described by PÉREZ-JIMÉNEZ & CALIXTO (2008). The FRAP assay was performed according to MOREIRA et al. (2005). Results were expressed as mmol of Fe⁺² equivalents per g or liter. Each sample was analyzed in triplicate. The TEAC assay was performed according to RE et al. (1999). Results were expressed as mmol of Trolox equivalents per g or liter. Each sample was analyzed in triplicate.

Incorporation of WIBP beads in beer

Just after being prepared, 0.32 g of WIBP beads were immersed in 10 mL wheat beer in 15 mL amber bottles, which were kept at room temperature for 60 days. One milliliter sample was withdrawn from beers containing WIBP beads after 15, 30 and 60 days of immersion and stored at -20 °C until analysis.

Extraction of soluble and insoluble phenolic compounds

To investigate whether phenolic compounds were released from beads to beer, beer samples were clarified by a procedure described by PERRONE et al. (2012). For the analysis of the WIBP, extraction of soluble and insoluble phenolic compounds was performed as described by DINELLI et al. (2011). The whole extraction process was performed in duplicate.

Phenolic compounds analysis

Phenolic compounds were analyzed by HPLC with diode array detector (DAD) (Shimadzu, Kyoto, Japan). Chromatographic separations were achieved using a Kromasil^® C18 column (5 μm, 250 mm × 4.6 mm i.d.) coupled to a Kromasil^® C-18 pre-column (5 μm, 10 mm × 3 mm) maintained at a constant temperature of 40 °C. The LC mobile system consisted of a gradient of water with 0.3% formic acid, methanol and acetonitrile, with a constant flow rate of 1.0 mL/min. Phenolic compounds were monitored by DAD between 190 to 370 nm and identified by comparison of their retention times and UV spectra with those of commercial standards. Quantification was performed by external standardization. Data were acquired by LCMS solution software (Shimadzu Corp., version 2.00, 2000). Results were expressed as mg/100 g. This methodology was validated by ALVES & PERRONE (2015).

Simulated digestion of WIBP beads

WIBP beads immersed for 60 days in the wheat beer were used to evaluate the bioaccessibility of phenolic compounds and their gut by simulated digestion. In vitro human gastrointestinal digestion: The in vitro human simulated gastrointestinal digestion, including the oral, gastric, and small intestine phases, was performed according to DA SILVA et al. (2019) with modifications. For the oral phase simulation, aliquots of 1 g of the WIBP beads were placed in a glass vial followed by the addition of 3 mL of human saliva, donated spontaneously by two volunteers, and incubated at 37 °C for 1 min under orbital agitation at 260 rpm. After the oral phase, a 2.5 mL aliquot of artificial gastric fluid was added to the vials, which were sealed with a rubber septum and the atmosphere was replaced by N₂. Vials were then incubated at 37 ºC for 2 h under orbital shaking at 260 rpm. After the gastric phase, the pH was adjusted to 6.0 with NaHCO₃ and 2.0 mL of artificial small intestine fluid were added to the vials, which resealed, and then the atmosphere was replaced by N₂. Vials were incubated at 37 ºC for 2 h under orbital shaking at 260 rpm. All steps were performed in triplicate and independently. At the end of each phase of digestion (oral, gastric, and small intestine), aliquots were collected and centrifuged (3000 g, 15 min, 25 °C). The supernatant was analyzed by HPLC-DAD as described in section 2.6. Ex vivo gut fermentation: The ex vivo gut fermentation was performed according to the methodology described by MOSELE et al. (2015), with modifications. The feces of one healthy volunteer were homogenized in a nutrient-rich medium (0.5 g in 10 mL), as described by MCDONALD et al. (2013), and 5.0 mL of this mixture were added to the material obtained after all three phases of digestion previously described, incubated at 37 ºC and 50 rpm for 4 h, 12 h and 48 h under anaerobiosis. All steps were performed in triplicate. Feces were donated by a volunteer who filled the following inclusion criteria: age between 18 and 35 years, eutrophic (body mass index from 18.5 to 24.9 kg/m²), no gastrointestinal disease, regular bowel function and without the use of nutritional supplements, antibiotics, probiotics, prebiotics or symbiotic in the three months prior to collection of feces. The volunteer was instructed to avoid, for at least two days prior to feces collection, the ingestion of foods rich in phenolic compounds, such as fruits in general, black beans, cabbage, juices, alcoholic beverages, soy and soy-derived products. The study protocol was approved by the Ethics and Research Committee (number 512847) of the Clementino Fraga Filho University Hospital at the Federal University of Rio de Janeiro. At the end of each time of ex vivo gut fermentation, aliquots were collected and centrifuged (3000 g, 15 min, 25 °C). The supernatant was analyzed by HPLC-DAD as described in section 2.7. Bioaccessibility (B) was calculated according to DE ALMEIDA et al. (2020), as follows:

B (%) = A/B × 100, in which A is the phenolic content (μg/g dry weigh of WIBP beads) of sample extract after each digestion step and B is the initial phenolic content (μg/g dry weigh of WIBP beads) estimated for the WIBP beads before the immersion in beer.

Statistical analysis

All of experiments were carried out in triplicate. Data were reported as means ± standard deviation. Differences among means were analyzed by one-way analysis of variance (ANOVA) followed by Tukey post-hoc multiple comparison test using Statistica software (version 7.0, StatSoft Inc., Tulsa, OK). Differences were considered significant when P < 0.05.

RESULTS AND DISCUSSION

Physical and morphological analysis of WIBP beads

WIBP beads were visually spherical and assumed the color of the WIBP (dark purple), as shown in figure 1A. SEM revealed a spherical shape of WIPB beads (Figure 1B) with a relatively rough surface and markedly open and large pores with craters bordered by prominent walls (Figure 1C). This morphology is like alginate beads reported in other studies (BITTENCOURT et al., 2018; DA COSTA NETO et al., 2019; LOTFIPOUR et al., 2012). No cracks were observed in the surface of the beads, which could increase erosion and promote a release of the phenolic compounds from the WIBP beads. Figure 2 shows the XRD patterns of sodium alginate (a), WIBP (b) and WIBP beads. The presence of crystalline regions with two broad peaks at 2θ = 13° and 23° (Figure 2A) was observed for sodium alginate, which is consistent with previously reported data (FONTES et al., 2013). These peaks match the lateral packing of alginate molecules and the layer spacing along the molecular chain direction, respectively (VREEKER et al., 2008). Regarding WIBP (Figure 2B), XRD reveals the presence of crystalline regions in one broad peak at 2θ of 21.7° and many evident peaks, which indicates the crystallinity intensity in this material. WIBP beads (Figure 2C) show XRD patterns depicting the disappearance of one alginate peak (2θ = 13º) and the intensity reduction of the other peak (2θ = 23º) after the formation of the beads (when alginate cross-links with Ca²⁺). The WIBP peaks, including the broad one, are also reduced when it is encapsulated by calcium alginate beads. This could be the result of the strong interaction between alginate and Ca²⁺, which disturbed the close packing of the alginate molecules for the formation of regular crystallites, as reported by CHO et al. (2014).

Figure 1
(A) Calcium alginate beads with wine industry by-product (WIBP): visually spherical and dark purple. (B,C) Scanning electron micrographs of calcium alginate beads with wine industry by-product (WIBP) at 43x (B) and 2000x (C) magnification.

Figure 2
X-ray diffraction patterns for sodium alginate (A), wine industry by-product (WIBP) (B) and WIBP beads (C).

Antioxidant activity

Phenolic compounds are considered very important antioxidant sources in beer. They also play critical roles both in flavor stability and in the colloidal stability of beer (VANDERHAEGEN et al., 2006). The antioxidant activity of the craft beer was 2.49 ± 0.06 mmol Trolox/L and 1.16 ± 0.09 mmol Fe²⁺/L when assessed by TEAC and FRAP assays, respectively. Although, both methods evaluate antioxidant activity, FRAP is generally based on electron transfer reaction mechanisms and TEAC is related to the transfer of hydrogen atoms and electrons simultaneously, thus resulting in different values (LI et al., 2012). MOURA-NUNES et al. (2016) reported that the antioxidant capacity of Brazilian beers varied between types and styles, ranging from 0.81 mmol Fe⁺²/L to 6.37 mmol Fe⁺²/L (FRAP) and 0.40 mmol Trolox/L to 3.02 mmol Trolox/L (TEAC). These results agree with the values obtained for the wheat beer in the present study. Pellegrini et al. (2003) evaluated the antioxidant capacity of alcoholic beverages from Italy and found 9 to 12 times higher antioxidant activities by TEAC and FRAP for red wines to a lager beer (1.04 mmol Trolox/L and 2.78 mmol Fe²⁺/L). The high antioxidant capacity of red wine is related to the prolonged contact between juice and pomace (PELLEGRINI et al., 2003) and is known for its health-protective effect on consumers (BERES et al., 2017). In this sense, it is interesting to evaluate if the addition of WIBP could increase the antioxidant activity of beers. The antioxidant activity of WIBP was 0.078 mmol Trolox/g and 0.13 mmol Fe²⁺/g when assessed by TEAC and FRAP assays, respectively. Pomaces remaining after vinification of six different grape varieties (Grenache, Syrah, Carignan Noir, Mourvèdre, Counoise and Alicante Bouchet) were analyzed by Ky et al. (2014) for their antioxidant activity and higher reducing power were found for seeds (0.176 - 0.267 mmol Fe²⁺/g), but for skins, Grenache (0.105 - 0.137 mmol Fe²⁺/g) and Counoise (0.122 mmol Fe²⁺/g) varieties were similar to our result on WIBP. Inferior values were found for grape pomace of Vitis vinifera L. var. ‘Monastrell’ (0.019 mmol Trolox Equivalent/g) (COSTA-PÉREZ et al., 2023). These differences can be attributed to the total phenolic compounds level present in the sample rather than the concentration of any individual compound, even if some compounds may contribute more than others (KY et al., 2014). Martins et al. (MARTINS et al., 2016) determined the reducing power by the FRAP method for red, white and mixed grape pomaces and verified a range of, approximately, 0.05 to 0.25 mmol Trolox Equivalent/g, with the mixed grape pomace presenting the lower values.

Phenolic compounds in WIBP and wheat beer

Ten different phenolic compounds were identified in WIBP (Table 1), eight of them as soluble (gallic, 2,4-dihydroxybenzoic, p-coumaric, caffeic, 3,4-dihydroxybenzoic, and syringic acids, rutin, and quercetin) and four as insoluble (gallic, 3,4-dihydroxybenzoic, 3,4-dihydroxyphenylacetic, and m-coumaric acids). Gallic and 3,4-dihydroxybenzoic acids were present in both fractions. Gallic acid was the most abundant phenolic compound (Table 1). ROCKENBACH et al. (2011) reported that gallic acid was detected in all the samples of pomaces from the vinification of grape varieties widely produced in Brazil (Cabernet Sauvignon, Merlot, Bordeaux and Isabel) and the highest concentration (18.68 mg/100 g) was present in the Bordeaux variety. The content of total phenolic compound in WIBP (3.2 mg/g, Table 1) was much lower than that found for red grape marc (22 mg/g), the organic waste from wine production (MOSCHONA & LIAKOPOULOU-KYRIAKIDES, 2018), which might be related to the extraction procedure (they used a sonication bath) or the method used to determine total phenolic content (they used Folin-Ciocalteu colorimetric method). TROŠT et al. (2016) found similar values to WIBP (present study) for Cabernet Sauvignon grape by-products (1.7 mg/g) using a similar extraction procedure and HPLC analysis. Different compositions of phenolic compounds in winery wastes (skins, seed, pomace, etc) from different cultivars have been reported, including anthocyanins, flavanols, flavonols, stilbenes (resveratrol) and phenolic acids (PINELO et al., 2005; SPIGNO & DE FAVERI, 2007; TROŠT et al., 2016). TROŠT et al. (2016) described interesting phenolic profiles from extracts from winery by-products, stating that the yields are influenced by grapevine cultivar and extraction conditions.

Table 1
Soluble and insoluble phenolic compounds (mg/100g) from wine industry by-product (WIBP).

Phenolic compounds	Content (mg/100 g)
--------------------------------Soluble-------------------------------
gallic acid	3.4 ± 0.1
3,4-dihydroxybenzoic acid	0.6 ± 0.1
p- coumaric acid	0.8 ± 0.02
5-caffeoylquinic acid	3.1 ± 0.3
2,4-dihydroxybenzoic acid	5.8 ± 0.6
syringic acid	7.9 ± 0.01
rutin acid	10.7 ± 1.0
quercetin acid	14.8 ± 1.7
------------------------------Insoluble-------------------------------
gallic acid	153.4 ± 1.4
3,4-dihydroxybenzoic acid	30.8 ± 8.7
3,4-dihidroxyphenylacetic acid	106.5 ± 4.0
m-coumaric	47.9 ± 6.4
Total Phenolic Compounds	321.25 ± 7.47

• Results expressed as mean ± standard deviation of three replicates.

When WIBP was encapsulated, a sample of the remaining solution was used to determine the content of phenolic compounds. No detectable amount of phenolics was found in this sample, indicating that all phenolic compounds were encapsulated. Six free phenolic compounds were identified in the wheat beer before the addition of the encapsulated WIBP (Table 2): gallic, 3,4-dihydroxyphenylacetic, 4-hydroxybenzoic, 2,4-dihydroxybenzoic, ferulic, and salicylic acids, with salicylic acid being the most abundant phenolic compound, corresponding to 50% of the total content. The content of total phenolic compounds (around 40 mg/L, Table 1) was higher than the average content reported for Brazilian beers (13 mg/L) (MOURA-NUNES et al., 2016). PIAZZON et al. (2010) showed a different phenolic profile for a wheat beer, with ferulic acid as the major compound (10.4 mg/L), accounting for more than 50% of the total phenolic compounds. This was the most abundant phenolic acid for 21 different commercial beers, from 9 different European countries (Germany, Belgium, Italy, The Netherlands, England, France, Austria, Czech Republic, and Ireland). Gallic acid was the most abundant phenolic compound in commercial Brazilian beers, as reported by MOURA-NUNES et al. (2016). According to ZHAO et al. (2010), in addition to gallic acid, ferulic acid was also abundant in Chinese commercial beers. Conversely, gallic acid was not reported in European beers (PIAZZON et al., 2010). The amount and quality of raw materials are dependent on the industrial brewing process, which can influence the phenolic compound contents (RODRIGUES & GIL, 2011).

Table 2
WHEAT BEER: Phenolic compounds (mg/L) in the wheat beer without wine industry by-product (WIBP) beads and with WIBP beads immersed for 15, 30 and 60 days and SIMULATED DIGESTION: Content (µg/g dry weight of WIBP beads) of individual phenolic compounds (PC) and Bioaccessibility (B, % in relation to PC in WIBP beads) during simulated digestion: oral digestion, gastric digestion, small intestine digestion, and ex vivo gut fermentation.

	-------------------------------------------------------------------------WHEAT BEER------------------------------------------------------------------------
	-------------------------------------------Phenolic compound content (mg/L)-------------------------------------------------
Phenolic compound	Wheat beer without WIBP	15 days		30 days		60 days
gallic acid	4.8 ± 0.1a	4.8 ± 0.1a		4.7 ± 0.1ab		4.4 ± 0.1b
3,4-dhPAacid	6.7 ± 0.2a	6.6 ± 0.2a		6.7 ± 0.1a		6.6 ± 0.1a
p-hB acid	7.3 ± 0.4a	7.2 ± 0.5a		7.2 ± 0.4a		7.0 ± 0.2a
2,4-dhB acid	1.9 ±0.1a	1.9 ± 0.1a		1.9 ± 0.1a		1.7 ± 0.03a
ferulic acid	0.5 ± 0.0a	0.7 ± 0.0a		0.7 ± 0.0a		0.4 ± 0.06a
salicylic acid	20.5 ± 1.5a	19.6 ±0.9a		19.3 ± 0.8a		18.7 ± 0,1a
Total	41.7 ± 0.71a	40.8 ± 0.53ab		40.5 ± 0.42ab		38.8 ± 0.56b
	-------------------------------------------------------------------SIMULATED DIGESTION----------------------------------------------------------------
Phenolic compound	WIBP beads2	Oral digestion			Gastric digestion		Small intestine digestion
	(µg/g)	(µg/g)	B (%)	(µg/g)	B (%)	(µg/g)	B (%)
Gallic acid	1140.4	ND	0	13.2d	1.2	64.3b	5.6
3,4-dhPA acid	774.5	ND	0	2.1b	0.3	15.9b	2.0
Quercetin	107.6	ND	0	ND	0	ND	0
Rutin	77.8	ND	0	ND	0	ND	0
3,4-dhB acid	228.4	ND	0	ND	0	ND	0
Syringic acid	57.4	ND	0	ND	0	ND	0
Total	2336.43	ND	0	15.3d	0.6	80.2c	3.4
Phenolic compound	--------------------------------------------Gut fermentation---------------------------------------------
	------------------4 h------------------		------------24 h------------		------------48 h------------
	(µg/g)	B (%)	(µg/g)	B (%)	(µg/g)	B (%)
Gallic acid	43.3c	3.8	71.6a	6.3	40.8c	3.6
3,4-dhPA acid	164.1a	21.2	5.0b	0.6	6.8b	0.9
Quercetin	6.0c	5.6	8.9b	8.3	40.0a	37.2
Rutin	ND	0	42.8b	55.0	45.7a	58.7
3,4-dhB acid	ND	0	2.5a	1.1	ND	0
Syringic acid	ND	0	3.3b	5.7	10.8a	18.8
Total	213.4a	9.1	134.1b	5.7	144.1b	6.2

• 3,4-dhPA acid: 3,4-dihidroxyphenylacetic acid; p-hB acid: p-hidroxybenzoic acid; 2,4-dhB acid: 2,4-dihydroxybenzoic acid. 3,4-dhB acid: 3,4-dihydroxybenzoic acid. WEAT BEER: Results expressed as mean ± standard deviation of two replicates. Different superscript letters in the same line indicate significant difference between samples (ANOVA followed by Tukey’s multiple comparison post hoc test, P < 0.05). SIMULATED DIGESTION: Different superscript letters in the same row indicate significant differences between samples (ANOVA followed by Tukey’s multiple comparison post hoc test, P < 0.05). ²Estimated considering data in table 1 and considering 4 g of WIBP in 5.5 g of WIBP beads; ³Considering data of table 1, other phenolic compounds were detected in WIBP, but not during simulated digestion. ND = not detected.

Release of phenolics to beer

The addition of WIBP beads to the wheat beer did not cause any change in the total phenolic compound contents of the beverage (Table 2). Moreover, no change in the phenolic compounds profile was observed in the beer with WIBP beads immersed for 60 days (Table 2). These results suggest that not only encapsulation retained WIBP phenolics when beads were immersed in the liquid, but beads were stable enough to avoid their leaching to the beverage during storage. MOSCHONA & LIAKOPOULOU-KYRIAKIDES (2018) also encapsulated wine by-products and tested the phenolic release into ethanol and buffer solutions. At room temperature, 15% to 25% of phenolic compounds were released to buffer and ethanol solutions, respectively, after 24 h. The WIBP encapsulation process used in the present study, including the concentration of alginate and CaCl₂, were previously optimized (VIEIRA et al., 2019) to reduce swelling and erosion of the beads, which may explain their high capacity to efficiently retain the phenolics from the core material.

Bioaccessibility of phenolic compounds

No phenolic compounds were released after the oral phase of digestion from the WIBP beads that were immersed in the wheat beer for 60 days (Table 2). Two phenolic compounds were detected after the gastric phase of digestion: gallic and 3,4-dihydroxyphenylacetic acids (Table 2). The same compounds were observed after the small intestine phase of digestion but at higher concentrations (Table 2), indicating a progressive release of phenolic compounds during simulated digestion, evidenced by the increase in bioaccessibility (B). These compounds detected after GD and SID are present mainly in the insoluble part of the WIBP (Table 1), suggesting that the physicochemical conditions of these digestion phases were able to release them from the matrix. LINGUA et al. (2018) detected gallic acid after oral and stomach digestion of grapes but did not detect it after the intestinal phase, which was attributed to the alkaline pH of the digestive fluid (LINGUA et al., 2018). In the case of WIBP beads, it seems that the alginate-calcium structure is protecting the phenolic compounds from these digestive conditions. In addition, it impeded its release after the oral digestion phase. ZHAO et al. (2013) reported that gastric juice, whose pH is around 2, caused the exchange of calcium by hydrogen ions in alginate cross-links of the beads, which could enhance the strength of their supramolecular structure. On the other hand, due to the increase in pH to above 8.1 in the small intestine, the release of phenolic compounds from the beads was fast. The bioaccessibility of total phenolic compounds was relatively low after the small intestine digestion (3.4 %, Table 2) in comparison to other grape/wine products found in literature (FERREYRA et al., 2021; JARA-PALACIOS et al., 2018; LINGUA et al., 2018). Although, this value increased at the beginning of simulated gut fermentation (9%, Table 2), as also reported by DE ALMEIDA et al. (2020), higher values are reported in the literature for other matrices. DE ALMEIDA et al. (2020) detected around 40% of bioaccessibility of total phenolics for bioprocessed bread with green coffee infusion after gut fermentation. The effect of the digestion process of bunch stems and grape cane extracts, by-products of the grapevine of the Malbec variety, were evaluated by FERREYRA et al. (2021), and the total PCs were 20 and 74 % bioaccessible, respectively. Values above 62% of bioaccessibility for phenolic acids were found for seed, skin, stem, and pomace extracts after simulated digestion (JARA-PALACIOS et al., 2018). The lower bioaccessibility of phenolic compounds from WIBP beads can be attributed to the Ca²⁺- alginate beads, which protect the core material, or even because the bioaccessibility value was calculated considering the initial content of the material, which, in turn, was estimated by the amount detected in WIBP. ALVES et al. (2021) found lower bioaccessibility values (4.8 times lower for gallic acid) when considering the content of phenolics in the initial material in comparison to bioaccessibility values considering the content in the previous digestion step.

After the gut fermentation, 3,4-dihydroxyphenylacetic acid was the most abundant phenolic compound (164.1 µg/g) in the first four hours. APPELDOORN et al. (2009) and CUEVA et al. (2013) proposed that the formation of 3,4-dihydroxyphenylacetic acid could be the result of the catabolism of dimeric procyanidins. However, in this case, the insoluble part of WIBP could be the source of this compound. Other compounds were also detected in this digestion stage, including quercetin, rutin, and syringic acid. These compounds were not found in the craft wheat beer (Table 2) but were present in the WIPB (Table 1), indicating a release of phenolic compounds from WIBP beads during gut fermentation. As far as we know, this is the first report in literature describing the addition of encapsulated wine waste to increase the phenolic content of beer, and that these compounds can be absorbed during gastrointestinal digestion. Additionally, the encapsulation of the wine waste to increase the health qualities of a drink helps to protect the active substances during the storage period to be released during the digestive processes. In this sense, the target nutrient is absorbed by the human organism, fulfilling the nutritional purpose of the encapsulation (FANG & BHANDARI, 2010).

CONCLUSION

The incorporation of encapsulated phenolic compounds into beer was observed for the first time in the present study. The red grape pomace (WIBP) used as core material for the beads was rich in antioxidants with high concentrations of phenolic compounds. These enriched beads were added to a craft wheat beer and the phenolic compounds were not released during the 60 days of storage, protecting the phenolic content and the antioxidant activity of the core material. The release of phenolic compounds from the beads during simulated digestion, especially of WIBP components that were not present in beer, shows the advantage of using these beads as enrichment material for beverages in general. But, certainly, sensorial analysis of the presence of these beds in beverages should be performed.

ACKNOWLEDGEMENTS

The authors gratefully thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (for Mr. Alves’s scholarship), and A Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (Brazil) for financial support. The authors also thank the finaltial support of Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brasil - Finance code 001.

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• CR-2024-0304.R1

BIOETHICS AND BIOSECURITY COMMITTEE APPROVAL

• The studies involving human participants were reviewed and approved by Research ethics committee of Clementino Fraga Filho Hospital from Federal University of Rio de Janeiro, Brazil (approval number 512.847). The patients/participants provided their written informed consent to participate in this study.

Edited by

• Editors: Rudi Weiblen (0000-0002-1737-9817) Cristiano Ragagnin de Menezes (0000-0003-4523-8875)

Publication Dates

• Publication in this collection
  20 Jan 2025
• Date of issue
  2025

History

• Received
  03 June 2024
• Accepted
  12 Aug 2024
• Reviewed
  14 Nov 2024