Bioaccessibility of Phenolic Acids and Flavonoids from Buckwheat Biscuits Prepared from Flours Fermented by Lactic Acid Bacteria
by
, , and
Henryk Zieliński
*
,
Wiesław Wiczkowski
,
Joanna Topolska
,
Mariusz Konrad Piskuła
and
Małgorzata Wronkowska
Division of Food Sciences, Department of Chemistry and Biodynamics of Food, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima 10, 10-748 Olsztyn, Poland
*
Author to whom correspondence should be addressed.
Molecules 2022, 27(19), 6628; https://doi.org/10.3390/molecules27196628
Submission received: 1 September 2022
/
Revised: 30 September 2022
/
Accepted: 4 October 2022
/
Published: 6 October 2022
(This article belongs to the Special Issue Bio-Accessibility/Availability of Bioactive Compounds from Natural Food Sources)
Abstract
:The literature reports that the consumption of common buckwheat (Fagopyrum esculentum Moench), exactly the polyphenols it contains, is associated with a wide spectrum of health benefits. Therefore, the determination of the bioaccessibility of phenolic acids and flavonoids from buckwheat biscuits formulated from liquid-state fermented flours (BBF) by selected lactic acid bacteria (LAB) after gastrointestinal digestion was addressed in this study. Bioaccessibility could be defined as the fraction of a compound that is released from the food matrix in the gastrointestinal lumen and used for intestinal absorption. The bioaccessibility of eight phenolic acids (protocatechuic, vanillic, syringic ferulic, caffeic, sinapic, p-coumaric, and t-cinnamic) and six flavonoids (epicatechin, vitexin, orientin, apigenin, kaempferol, and luteolin) were provided for BBF and BBC (buckwheat biscuits prepared from fermented and unfermented flours, respectively). The bioaccessibility indexes (BI) indicated the high bioaccessibility of phenolic acids and improved bioaccessibility of flavonoids from BBF. Moreover, the data provide evidence for the suitability of selected LAB strains to be used as natural sour agents for further bakery product development rich in phenolic acids and flavonoids with LAB-dependent bioaccessibility.
1. Introduction
Common buckwheat is known as a gluten-free pseudocereal utilized worldwide, while other species are used as a traditional food in some regions such as south of China, Bhutan, the Himalayan hill region from northern Pakistan to eastern Tibet, and in Islek, Europe [1]. The common buckwheat is regularly consumed as raw or roasted groats, or as breakfast cereals, in various bakery products, and enriched non-bakery products (tea, honey, tarhana, sprouts) [2]. Because buckwheat does not contain gluten, it can be consumed by people with celiac disease [3]. The consumption of buckwheat-based products is related to a wide range of biological and healthy activities, such as hypocholesterolemic, hypoglycemic, anticancer, and anti-inflammatory, and buckwheat proteins and antioxidant phenolic compounds, such as phenolics, are presumed to be responsible, at least in part, for these benefits [3,4,5].
A new trend of cereal processing is natural and inoculated fermentation offering a wide range of derived fermented products. The fermentation processes, depending on the water content in the system, can be divided into solid- (SSF) and liquid-state fermentation (LSF). The positive aspects of cereal fermentation include the degradation of antinutrients but also increasing the nutritional value and availability of minerals, proteins, or carbohydrates [5,6,7]. Fermentation of cereals or pseudocereals is carried out mainly by lactic acid bacteria (LAB). An improvement in sensory and baking qualities was demonstrated as a result of the use of sourdough, which, through LAB metabolism, allowed us to obtain a product with an attractive flavor and texture [8]. Extended shelf life or new ingredients formed during the fermentation process are beneficial features of fermented products. However, despite these benefits, there are few reports of the effects of fermentation on plant secondary metabolites and related antioxidant properties [9]. We showed that LSF caused a slight specific LAB-dependent increase in total phenolic compounds, thus, providing evidence for the suitability of selected LAB strains to be used as natural sour agents for further bakery product development [10].
The previous study showed the average levels of phenolic acids and flavonoids in unfermented buckwheat flour, fermented flours, and water biscuits before and after in vitro digestion [11]; however, the bioaccessibility of the identified phenolic acids and flavonoids from BBF, despite the rutin and quercetin described bioaccessibility [12], was not investigated in relation to the specific LAB strain used for LSF. Bioaccessibility could be defined as the fraction of a compound that is released from the food matrix in the gastrointestinal lumen and used for intestinal absorption [13]. From a nutrition perspective, the measurement of bioaccessibility provides valuable information for selecting the source of food matrices to ensure the nutritional efficacy of food products [14].
Recently, we studied the multifunctionality of buckwheat biscuits (BBF) baked from common buckwheat flours after liquid-state fermentation (LSF) by select lactic acid bacteria (LAB). The high bioaccessible anti-AGEs activity was found after digestion in vitro of BBF, which was positively correlated with the total phenolic compound bioaccessibility [15]. Moreover, we showed a low level of the ACE inhibitory activity of BBF and BBC, which was significantly increased after digestion. High significant correlations were found between inhibition of ACE (IC50) and total phenolic compounds of BBF before and after digestion, thus, indicating a link between phenolic compound content and ACE inhibitory activity [11].
Therefore, this study aimed to investigate the potential bioaccessibility of individual phenolic acids and flavonoids from BBF prepared from flours fermented by selected lactic acid bacteria (L. acidophilus (145, La5, V), L. casei (LcY, 2K), L. delbruecki subsp. bulgaricus (151, K), L. plantarum (W42, IB), L. rhamnosus (GG, 8/4, K), L. salivarius AWH, Streptococcus thermophilus Mk-10) after an in vitro digestion procedure that mimics the physiochemical changes occurring in gastric and small intestinal digestion.
2. Results
2.1. Bioaccessibility of Phenolic Acids
In this study, the content of the phenolic acids identified in BBF and BBC buckwheat biscuits before and after in vitro digestion was provided. The eight phenolic acids known as derivatives of hydroxycinnamic acid (ferulic, caffeic, sinapic, p-coumaric, t-cinnamic) and derivatives of hydroxybenzoic acid (protocatechuic, vanillic, syringic) were identified. Among phenolic acids, vanillic, protocatechuic, and syringic acids were predominant. The level of phenolic acids (μg/g DM) in BB before and after digestion in vitro is presented in Table 1 and Table 2, respectively.
Having the content of phenolic acids (μg/g DM) in buckwheat biscuits prepared from unfermented (BBC) and fermented flours (BBF) by selected lactic acid bacteria before and after in vitro digestion, the bioaccessibility indexes (BI) of phenolic acids were calculated, and they are shown in Table 3.
The content of vanillic acid in BBF prepared from fermented flours ranged from 75 to 129 μg/g DM compared with 112 μg/g DM noted in the control BBc (Table 1). Digestion of biscuits led to an increase in the content of vanillic acid, and it was almost two-threefold higher for both BBF and BBC (Table 2). The bioaccessibility index (BIvanillic) for both BBF and BBC was >1, indicating high bioaccessibility of vanillic acid. BIvanillic ranged from 1.77 to 3.22 compared with the 1.67 obtained for BBc. The highest BIvanillic was found for BBF baked from flour fermented by L. plantarum W42 and L. rhamnosus K (Table 3).
The protocatechuic acid was found in BBF within the range of 39–85 μg/g DM compared to 65 μg/g DM noted in BBc (Table 1). After digestion of BBF, its content increased 4–7 times, whereas a threefold higher content was noted in digested BBc (Table 2). The bioaccessibility index (BIprotocatechuic) for BBF was >3, thus, indicating for very high bioaccessibility of this acid. BIprotocatechuic ranged from 2.90 to 7.79 compared with 3.09 obtained for BBC. The highest BIprotocatechuic was found for BBF formulated on fermented flours by L. rhamnosus 8/4 and L. salivarius AWH (Table 3).
The syringic acid was present in BBC and BBF at a concentration at least threefold lower than the most abundant vanillic acid. It ranged widely from 21 to 159 μg/g DM compared with 43 μg/g DM noted in BBC (Table 1). After digestion of BBF, its content increased significantly (Table 2), resulting in high BIsyringic ranging from 2.07 to 10.83 compared with 2.99 obtained for BBC.
The not predominant phenolic acids included para-coumaric, sinapic, trans-cinnamic, caffeic, and ferulic acid, and the following observations were drawn on the basis of their content in BBF and BBC before digestion (Table 1). The content of these acids in BBC was from 3.4 μg/g DM (caffeic acid) up to 21.5 μg/g DM (para-coumaric) compared with the lowest content of 1.4 μg/g DM noted for caffeic acid in BBF by L. rhamnosus 8/4, and the highest one of 28.5 μg/g DM found for para-coumaric acid in BBF by L. rhamnosus K. Generally, the content of these acids noted in BBF was decreased or not changed. There were noted some exceptions made to the selected LAB strain used for flour fermentation, where a significant increase was noted for para-coumaric in BBF by L. rhamnosus K, for sinapic acid by L. casei 2K, for trans-cinnamic by L. plantarum W42, and for caffeic and ferulic acid in BBF by L. casei 2K. Since the baking conditions were the same for BBC and BBF, it is indicated for the impact of the selected LAB on the phenolic acid contents. When the total content of phenolic acids was considered, the flour fermented by L. rhamnosus K offered the highest content in BBF, higher by almost 59% compared with their content in BBC.
In this study, it was found that the digestion of BBF and BBC led to an increase in the content of p-coumaric acid compared with undigested biscuits (Table 2). BIp-coumaric for BBF ranged from 1.06 to 5.66 compared with 1.22 noted for BBC (Table 3). The highest BIp-coumaric was found for BBF formulated on fermented flours by L. rhamnosus 8/4. Similar findings were found for BIsinapic, BIt-cinnamic, and BIferulic, with the highest BI for BBF formulated on fermented flours by L. plantarum W42 (21.79), Streptococcus thermophilus MK-10 (9.15), and by L. rhamnosus GG (4.57), respectively (Table 3). The widest range of BI was noted for caffeic acid in BBF as it ranged from 3.80 up to 31.32 for fermented flours by L. rhamnosus 8/4. In summary, the digestion in vitro released all phenolic acids in BBF, as is well seen when the average BI is compared to their BI for BBC (Table 3).
2.2. Bioaccessibility of Flavonoids
In this study, despite rutin- (quercetin-3-rutinoside) and quercetin-described bioaccessibility in our previous study [12], seven other flavonoids before and after digestion in vitro were identified in BBF and BBC, including epicatechin, vitexin, orientin, apigenin, kaempferol, and luteolin (Table 4 and Table 5, respectively).
The bioaccessibility of flavonoids provided in detail (Table 6) is based on their content in BBF and BBC before and after digestion in vitro.
The epicatechin was the major flavonoid found in BBF in a wide range from 17.9 to 127.6 μg/g DM, depending on the LAB strain used for flour fermentation compared with 91.7 μg/g DM noted for BBC (Table 4). It was also found that BBF contained about threefold lower epicatechin content than BBC, with the exception of biscuits baked from fermented flours by L. rhamnosus 8/4, L. rhamnosus K, and L. salivarius AWH. The differential behavior of epicatechin was noted after digestion of BBF, as in some cases, epicatechin was released from BBF, or no changes were observed. However, the epicatechin level in BBF after digestion was increased compared with its level in BBC (Table 5). Therefore, the average BIepicatechin for BBF was 1.04, and it was almost five times higher compared with its value for BBC. The highest BIepicatechin was noted for BBF prepared from flours fermented by L. acidophilus V and L. acidophilus 145 (Table 6).
A similar trend was noted for vitexin, orientin, apigenin, and luteolin; however, their content in BBF was lower than epicatechin. Their BI indexes were higher than one, indicating the high bioaccessibility in contrast to the BI value lower than one noted for BBC. The opposite data were provided for kaempferol since its content was decreased after digestion of both BBF and BBC (Table 5), but its bioaccessibility was still very high (Table 6).
As shown in Figure 1, all LAB strains used for buckwheat flour fermentation, despite L. casei LcY and Streptococus thermophilus MK-10, offered a buckwheat dough matrice from which phenolic acids and flavonoids were easier released into digestion fluid. It was noted that phenolic acids formed the main fraction after digestion in vitro compared with flavonoids.
3. Discussion
3.1. Bioaccessibility of Phenolic Acids
There is an increasing interest in a healthy lifestyle and the consumption of substantial portions of secondary plant metabolites, such as polyphenols, because of their benefits for the human body. As human studies are time-consuming, costly, and restricted by ethical concerns, in vitro models for investigating the effects of digestion on these compounds have been developed to predict their release from the food matrix, as well as their bioaccessibility [16]. The most widely used procedure for screening polyphenolic compound bioaccessibility is the in vitro static GI method [17]. Contrary evidence on the bioaccessibility of phenolic compounds is available in the literature. Carbonell-Capella et al. [17] showed that gastric digestion increased polyphenolic concentration, whereas the duodenal fraction significantly diminished polyphenolic content. In contrast, Tagliazucchi et al. [18] observed an increase in the bioaccessibility of total polyphenols, flavonoids, and anthocyanins during the gastric digestion in grapes, while intestinal digestion caused a decrease in all classes of polyphenols.
It was shown that in vitro digestion released much higher levels of total phenolic compounds (TPC) from biscuits obtained from fermented buckwheat flour compared with biscuits before digestion, which indicated a much better extraction system for phenolic compounds, which was the digestion fluid, compared with the classical extraction [11]. Generally, an increase in the potential bioaccessibility of TPC was observed. As a consequence, the individual phenolic compounds responsible for this increase in the bioaccessibility of TPC should be indicated. The data on the bioaccessibility of phenolic acids from the buckwheat matrix modified by the use of fermented flour for baking are still limited. In this study, it was shown that vanillic, protocatechuic, and syringic acids were predominant in buckwheat biscuits (control and obtained from fermented flour). Previously it was shown that the baking of BBF and BBC resulted in a reduction in the average content of phenolic acids [11]. Heat treatment may enhance polyphenol bioaccessibility because of disruption of plant tissue and denaturation of polyphenols–polysaccharide complexes. However, heat treatment may also cause thermal degradation of phenolic compounds [19]. As was presented in the review by Wojtunik-Kulesza et al. [20] during consideration of in vitro bioaccessibility studies, chemical and biochemical reactions or physical constraints occurring within food must be taken into account. Additionally, the release from the food matrix, particle size or pH-dependent transformations, and interactions between polyphenols and food components should be taken into account. For example, it was shown that the bioaccessibility of sinapic acid from bran-rich bread was much higher than that of ferulic acid and para-coumaric acid [21]. However, most phenolic compounds remain stable during salivary and gastric digestion [22]. Managa et al. [23] demonstrated that lactic acid bacteria used for fermentation of a smoothie composed of pineapple and chayote leaves increase the total phenol. These authors found that after in vitro digestion, fermentation improved the total phenol recovery by 66% during the intestinal phase compared with the control sample. After digestion, the TPC of mango juices decreased, while LAB-fermentation improved its bioaccessibility [24]. Bloem et al. [25] showed that Oenococcus oeni was not able to convert vanillic acid into vanillin. Micro-organisms, such as yeast, are also able to metabolize vanillin to vanillic acid or vanillyl alcohol by oxidoreductase enzymes [26]. Phelps and Young [27] demonstrated that the plant phenolic compounds ferulic and syringic acid were readily degraded by consortia of bacteria from this site under methanogenic, sulfidogenic, and denitrifying conditions.
3.2. Bioaccessibility of Flavonoids
Since the beneficial health effects of flavonoids depend on their absorption in the gut [28,29], their bioaccessibility is important to indicate their possible influence on the human organism. Rutin is the main buckwheat flavonoid, whereas quercetin is present in significantly lower concentrations [30], and our previous investigation showed that fermentation, baking, and in vitro digestion significantly affect their content [12]. It was found that the expanded bioaccessibility of rutin from BBF was low, and the BI of quercetin was greater than 1. Payne et al. [31] found that epicatechin, compared with catechin, is as much as 30 times greater in fresh and dried cocoa beans, but as conventional processing occurs, there is a loss in epicatechin and, at times, an increase in catechin.
Choi et al. [32] showed that the total flavonoid contents of the various buckwheat food matrices were higher after digestion compared with the predigested form, which indicated that flavonoids are easily released by in vitro digestion. These authors found that processed buckwheat samples had improved flavonoid bioaccessibility upon baking, which indicated that they are easily released from the food matrix by both digestion and baking. A significant increase of 7 out of 11 flavonoid compounds after in vitro gastrointestinal digestion of quinoa products was presented by Balakrishnan and Schneider [33]. Thilakarathna and Rupasinghe [34], in the review, showed that flavonoids had shown promising health-promoting effects in human cell culture, experimental animal, and human clinical studies. Still, an investigation is required to enhance the bioavailability and subsequent efficacy of certain flavonoids using consumer-friendly technologies.
4. Materials and Methods
4.1. Chemicals
Reagents in MS grade, including acetonitrile, methanol, water, and formic acid, were purchased from Sigma Chemical Co. (St. Louis, MO, USA). While diethyl ether (Et2O), hydrochloric acid (HCl), and sodium hydroxide (NaOH) were obtained from POCH S.A. (Gliwice, Poland). Compound standards (phenolic acids, flavonoids) were purchased from Sigma Chemical Co. (St. Louis, MO, USA) and Extrasynthese (Genay, France) and were used for identification and calculation.
4.2. Fermentation of Buckwheat Flours by LAB, Preparation of Buckwheat Biscuits from Fermented Flours (BBF), and In Vitro Digestion of BBF
4.2.1. Buckwheat Flour
Buckwheat flour originating from commercial Polish common buckwheat (Fagopyrum esculentum Moench) was purchased from local industry (Melvit S.A., Kruki, Poland). According to the produced declaration, the carbohydrate, dietary fiber, proteins, and fat content of buckwheat flour and roasted buckwheat groats were 62%, 2.3%, 7.2%, and 0.7% on a dry basis, respectively. Before fermentation, the buckwheat flour was pretreated as follows: about 50 g of flour was suspended with 950 mL of distilled water, heated at 90 °C for 45 min, then autoclaved at 121 °C for 15 min, and finally cooled to 37 °C. The pretreatment was carried out to reduce microbial populations in buckwheat flour before fermentation since they would compete with and inhibit the growth of inoculated microbes during the fermentation process.
4.2.2. Fermentation of Buckwheat Flours
The following selected lactic acid bacteria were used: L. acidophilus (145, La5, V); L. casei (LcY, 2K); L. delbruecki subsp. bulgaricus (151, K); L. plantarum (W42, IB); L. rhamnosus (GG, 8/4, K); L. salivarius AWH and Strepcococcus thermophilus Mk-10, all strains originated from the Institute of Animal Reproduction and Food Research of Polish Academy of Sciences’ collections. The Lactobacillus rhamnosus GG was purchased from ATCC®. Fermentation of buckwheat flours was carried out as follows: the 5% suspension of pretreated buckwheat flour in distilled water was inoculated with selected lactic acid bacteria with an amount of 8.00 log CFU/mL, and fermentation was performed at 37 °C for 24 h. The pretreated buckwheat flour not subjected to a fermentation process was used as a control sample. After fermentation, the samples were freeze-dried (Christ—Epsilon 2-6D LSC plus, Germany).
4.2.3. Preparation of BBF from Fermented Flour
The biscuit dough was prepared according to the AACC 10–52 method [35], with the modification proposed by Hidalgo and Brandolini [36]. The dough was cut with a square cookie cutter (60 mm). BBs were baked at 220 °C for 30 min (electric oven DC-21 model, Sveba Dahlen AB, Fristad, Sweden). The control biscuits (BBc) were formulated on unfermented buckwheat flour. The buckwheat biscuits were lyophilized, milled, and stored in a refrigerator until analysis.
4.2.4. In Vitro Digestion of Buckwheat Biscuits
The BBF and BBC were in vitro digested as described by Delgado-Andrade et al. [37] with some modifications [38]. Briefly, the three steps of digestion were saliva (pH 7.0), gastric (pH 2.0), and intestinal digestion (pH 7.5). Briefly, 10 g of lyophilized and milled buckwheat biscuits was suspended in 80 mL of deionized water. An α-amylase solution (77 U/mg solid) was added to the samples at a proportion of 3.25 mg/10 g of sample dry matter (d.m.) in 1 mM CaCl2, pH 7.0. Then, samples were shaken in a water bath at 37 °C for 30 min. For gastric digestion, the pH was reduced to 2.0 with 6 N HCl, and pepsin solution (738 U/mg) was added in the amount of 0.5 g/10 g of sample d.m. in 0.1 N HCl. The incubation was continued under the same conditions for 120 min. In the next step, the pH was adjusted to 6.0 with 6 M NaOH, and a mixture of pancreatin (activity 8xUSP) and bile salts extract was added. Subsequently, the pH was increased to 7.5 with 6 M NaOH, and water buffering to a pH of 7.5 was introduced to obtain a final volume of 150 mL. Then, the samples were incubated at 37 °C for 120 min. After incubation, the digestive enzymes were inactivated by heating at 100 °C for 4 min and cooled for centrifugation at 5000 rpm for 60 min at 4 °C in an MPV-350R centrifuge (MPW Med. Instruments, Warsaw, Poland). The supernatants obtained were stored at −18 °C for the evaluation of the bioaccessibility of phenolic acids and flavonoids from water biscuits.
4.3. Extraction, Isolation, and HPLC Analysis of Phenolic Compounds from BBF before and after In Vitro Digestion
The analysis of polyphenols (phenolic acids and flavonoids) was conducted according to the modified method of Wiczkowski et al. [39]. In the first step, about 0.05 g of freeze-dried samples was extracted 5 times with 80% MeOH. Next, polyphenolic compounds (forms released from soluble esters and soluble glycosides as well as free forms) were separated from the methanolic extracts in several stages. In the case of free forms of polyphenols, after adjusting the primary extract to pH 2 with 6 M HCl, the isolation by diethyl ether was carried out. However, in the case of conjugated forms (esters and glycosides), before adjusting the extract to pH 2 and the extraction of released forms of polyphenols by diethyl ether, the hydrolysis under a nitrogen atmosphere was executed for 4 h at room temperature with 4 M NaOH and subsequently in the condition of 6 M HCl for 1 h at 100 °C. After each hydrolysis, the extraction process was conducted in triplicates by utilizing sonication and centrifugation, and the collected ether extracts were evaporated to dryness under a nitrogen atmosphere at 35 °C. For the analysis of the profile and content of phenolic acids and flavonoids, the HPLC system (LC-200, Eksigent, Vaughan, ON, Canada) coupled with a mass spectrometer (QTRAP 5500, AB Sciex, Vaughan, ON, Canada) consisting of a triple quadrupole, ion trap, and ion source of electrospray ionization (ESI) was used. The chromatographic separation was conducted with a HALO C18 column (50 mm × 0.5 mm × 2.7 μm, Eksigent, Vaughan, ON, Canada) at 45 °C, at the flow rate of 15 μL/min. Identification and quantitation of the phenolic acids and flavonoids were based on the comparison of their retention times and the presence of the respective parent and daughter ion pairs (Multiple Reaction Monitoring method, MRM) with data obtained after analysis of the authentic standards.
4.4. Calculation of the Bioaccessibility Index of Phenolic Compounds
In this study, we determined the bioaccessibility index (BI) [38] of individual phenolic acids and flavonoids, which was calculated according to the following formulas:
where PAGD is the indicated phenolic acid content after simulated gastrointestinal digestion (GD), FGD is indicated flavonoid content after simulated gastrointestinal digestion (GD), PABB is the indicated phenolic acid content in BB, and FBB is indicated flavonoid content in BB. BIPA and BIF values > 1 indicate high bioaccessibility of phenolic acids and flavonoids from BB (BBF and BBC); BIFA and BIF values < 1 indicate low bioaccessibility.
BIPA = PAGD/FABB and BIF = FGD/FBB
4.5. Statistical Analysis
Results are given as the average ± standard deviation (SD) of n = 3 independent experiments. They were determined by one-way analysis of variance (ANOVA) with Fisher’s least significant difference test (p < 0.05). All analyses were made using STATISTICA for Windows (StatSoft Inc., Tulsa, OK, USA, 2001).
5. Conclusions
The bioaccessibility indexes of phenolic acids and flavonoids from buckwheat biscuits formulated from flours fermented by selected LAB are important factors in understanding the bioavailability of these compounds. The eight phenolic acids (protocatechuic, vanillic, syringic, ferulic, caffeic, sinapic, p-coumaric, and t-cinnamic) and seven other flavonoids than rutin and quercetin, including epicatechin, vitexin, orientin, apigenin, kaempferol, and luteolin were identified in buckwheat biscuits before and after digestion in vitro. The obtained data indicated the high bioaccessibility of phenolic acids and improved bioaccessibility of flavonoids under the influence of the fermentation and baking processes used. The study provides evidence for the suitability of selected LAB strains to be used as natural selected sour agents for further bakery product development rich in indicated phenolic acids and flavonoids with high bioaccessibility.
Author Contributions
Conceptualization, H.Z.; data curation, W.W., J.T. and M.W.; formal analysis, W.W. and J.T.; funding acquisition, H.Z.; methodology, H.Z.; project administration, H.Z.; software, W.W.; supervision, H.Z.; writing—original draft, H.Z., W.W., M.K.P. and M.W.; writing—review and editing, H.Z. All authors have read and agreed to the published version of the manuscript.
Funding
This work was supported by grant No 2014/15/B/NZ9/04461 from the National Science Centre, Poland. The APC was funded by the research funds of the Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences.
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
Data sharing is not applicable.
Conflicts of Interest
The authors declare no conflict of interest.
Sample Availability
Not available.
References
- Gimenez-Bastida, J.A.; Zieliński, H. Buckwheat as a functional food and its effects on health. J. Agric. Food Chem. 2015, 63, 7896–7913. [Google Scholar] [CrossRef] [PubMed]
- Gimenez-Bastida, J.; Piskuła, M.; Zieliński, H. Recent Advances in Processing and Development of Buckwheat Derived Bakery and Non-Bakery Products—A Review. Pol. J. Food Nutr. Sci. 2015, 65, 9–20. [Google Scholar] [CrossRef] [Green Version]
- Saturni, L.; Ferretti, G.; Bacchetti, T. The gluten-free diet: Safety and nutritional quality. Nutrients 2010, 2, 16–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Z.; Zhou, M.; Tang, Y.; Li, F.; Tang, Y.; Shao, J.; Xue, W.; Wu, Y. Bioactive compounds in functional buckwheat food. Food Res. Int. 2012, 49, 389–395. [Google Scholar] [CrossRef]
- D’Archivio, M.; Filesi, C.; Varì, R.; Scazzocchio, B.; Masella, R. Bioavailability of the polyphenols: Status and controversies. Int. J. Mol. Sci. 2010, 11, 1321–1342. [Google Scholar] [CrossRef]
- Simwaka, J.E.; Chamba, M.V.M.; Huiming, Z.; Masamba, K.G.; Luo, Y. Effect of fermentation on physicochemical and anti-nutritional factors of complementary foods from millet, sorghum, pumpkin and amaranth seed flours. Int. Food Res. J. 2017, 24, 1869–1879. [Google Scholar]
- Coda, R.; Di Cagno, R.; Gobbetti, M.; Rizzello, C.G. Sourdough lactic acid bacteria: Exploration of non-wheat cereal-based fermentation. Food Microbiol. 2014, 37, 51–58. [Google Scholar] [CrossRef]
- Wronkowska, M.; Jeliński, T.; Majkowska, A.; Zieliński, H. Physical properties of buckwheat water biscuits formulated on fermented flours by selected lactic acid bacteria. Pol. J. Food Nutr. Sci. 2018, 68, 25–31. [Google Scholar] [CrossRef]
- Dordevic, T.M.; Siler-Marinkovic, S.S.; Dimitrijevic-Brankovic, S.I. Effect of fermentation on antioxidant properties of some cereals and pseudo cereals. Food Chem. 2010, 119, 957–963. [Google Scholar] [CrossRef]
- Zieliński, H.; Szawara-Nowak, D.; Bączek, N.; Wronkowska, M. Effect of liquid-state fermentation on the antioxidant and functional properties of raw and roasted buckwheat flours. Food Chem. 2019, 271, 291–297. [Google Scholar] [CrossRef]
- Zieliński, H.; Honke, J.; Topolska, J.; Bączek, N.; Piskuła, M.K.; Wiczkowski, W.; Wronkowska, M. ACE inhibitory properties and phenolics profile of fermented flours and baked and digested biscuits from buckwheat. Foods 2020, 9, 847. [Google Scholar] [CrossRef] [PubMed]
- Zieliński, H.; Wiczkowski, W.; Honke, J.; Piskuła, M.K. In vitro expanded bioaccessibility of quercetin-3-rutinoside and quercetin aglycone from buckwheat biscuits formulated from flours fermented by lactic acid bacteria. Antioxidants 2021, 10, 571. [Google Scholar] [CrossRef] [PubMed]
- Rein, M.J.; Renouf, M.; Cruz-Hernandez, C.; Actis-Goretta, L.; Thakkar, S.K.; da Silva Pinto, M. Bioavailability of bioactive food compounds: A challenging journey to bioefficacy. Br. J. Clin. Pharmacol. 2013, 75, 588–602. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernandez-Garcia, E.; Carvajal-Lerida, I.; Perez-Galvez, A. In vitro bioaccessibility assessment as a prediction tool of nutritional efficiency. Nutr. Res. 2009, 29, 751–760. [Google Scholar] [CrossRef]
- Zieliński, H.; Szawara-Nowak, D.; Wronkowska, M. Bioaccessibility of anti-AGEs activity, antioxidant capacity and phenolics from water biscuits prepared from fermented buckwheat flours. LWT-Food Sci. Technol. 2020, 123, 109051. [Google Scholar] [CrossRef]
- Wojtunik-Kulesza, K.; Oniszczuk, A.; Oniszczuk, T.; Combrzyński, M.; Nowakowska, D.; Matwijczuk, A. Influence of In Vitro Digestion on Composition, Bioaccessibility and Antioxidant Activity of Food Polyphenols—A Non-Systematic Review. Nutrients 2020, 12, 1401. [Google Scholar] [CrossRef]
- Carbonell-Capella, J.M.; Buniowska, M.; Barba, F.J.; Esteve, M.J.; Frıgola, A. Analytical Methods for Determining Bioavailability and Bioaccessibility of Bioactive Compounds from Fruits and Vegetables: A Review. Compr. Rev. Food Sci. Food Saf. 2014, 13, 155–171. [Google Scholar] [CrossRef]
- Tagliazucchi, D.; Verzelloni, E.; Bertolini, D.; Conte, A. In vitro bio-accessibility and antioxidant activity of grape polyphenols. Food Chem. 2010, 120, 599–606. [Google Scholar] [CrossRef]
- Aherne, S.A.; Daly, T.; Jiwan, M.A.; O’Sullivan, L.; O’Brien, N.M. Bioavailability of β-carotene isomers from raw and cooked carrots using an in vitro digestion model coupled with a human intestinal Caco-2 cell model. Food Res. Int. 2010, 43, 1449–1454. [Google Scholar] [CrossRef]
- Bouayed, J.; Deußer, H.; Hoffmann, L.; Bohn, T. Bioaccessible and dialysable polyphenols in selected apple varieties following in vitro digestion vs. their native patterns. Food Chem. 2012, 131, 1466–1472. [Google Scholar] [CrossRef]
- Hemery, Y.M.; Anson, N.M.; Havenaar, R.; Haenen, G.R.M.M.; Noort, M.W.J.; Rouau, X. Dry-fractionation of wheat bran increases the bioaccessibility of phenolic acids in breads made from processed bran fractions. Food Res. Int. 2010, 43, 1429–1438. [Google Scholar] [CrossRef]
- Gayoso, L.; Claerbout, A.S.; Calvo, M.I.; Cavero, R.Y.; Astiasarán, I.; Ansorena, D. Bioaccessibility of rutin, caffeic acid and rosmarinic acid: Influence of the in vitro gastrointestinal digestion models. J. Funct. Foods 2016, 26, 428–438. [Google Scholar] [CrossRef]
- Managa, M.G.; Akinola, S.A.; Remize, F.; Garcia, C.; Sivakumar, D. Physicochemical Parameters and Bioaccessibility of Lactic Acid Bacteria Fermented Chayote Leaf (Sechium edule) and Pineapple (Ananas comosus) Smoothies. Front. Nutr. 2021, 8, 649189. [Google Scholar] [CrossRef] [PubMed]
- Cele, N.P.; Akinola, S.A.; Shoko, T.; Manhevi, V.E.; Remize, F.; Sivakumar, D. The Bioaccessibility and Antioxidant Activities of Fermented Mango Cultivar Juices after Simulated In Vitro Digestion. Foods 2022, 11, 2702. [Google Scholar] [CrossRef] [PubMed]
- Bloem, A.; Bertrand, A.; Lonvaud-Funel, A.; de Revel, G. Vanillin production from simple phenols by wine-associated lactic acid bacteria. Lett. Appl. Microbiol. 2007, 44, 62–67. [Google Scholar] [CrossRef]
- Fitzgerald, D.J.; Stratford, M.; Narbad, A. Analysis of the inhibition of food spoilage yeasts by vanillin. Int. J. Food Microbiol. 2003, 86, 113–122. [Google Scholar] [CrossRef]
- Phelps, C.D.; Young, L.Y. Microbial Metabolism of the Plant Phenolic Compounds Ferulic and Syringic Acids under Three Anaerobic Conditions. Microb. Ecol. 1997, 33, 206–215. [Google Scholar] [CrossRef]
- Saura-Calixto, F.; Serrano, J.; Goñi, I. Intake and bioaccessibility of total polyphenols in a whole diet. Food Chem. 2009, 101, 492–501. [Google Scholar] [CrossRef] [Green Version]
- Williamson, G.; Kay, C.D.; Crozier, A. The Bioavailability, Transport, and Bioactivity of Dietary Flavonoids: A Review from a Historical Perspective. Compr. Rev. Food Sci. Food Saf. 2018, 17, 1054–1112. [Google Scholar] [CrossRef] [Green Version]
- Zielińska, D.; Szawara-Nowak, D.; Zieliński, H. Comparison of spectrophotometric and electrochemical methods for the evaluation of the antioxidant capacity of buckwheat products after hydrothermal treatment. J. Agric. Food Chem. 2007, 55, 6124–6131. [Google Scholar] [CrossRef]
- Payne, M.J.; Hurst, W.J.; Miller, K.B.; Rank, C.; Stuart, D.A. Impact of fermentation, drying, roasting and dutch processing on epicatechin and catechin content of cacao beans and cocoa ingredients. J. Agric. Food Chem. 2010, 58, 10518–10527. [Google Scholar] [CrossRef] [PubMed]
- Choi, A.S.; Bea, I.Y.; Lee, H.G. Predicting buckwheat flavonoids bioavailability in different food matrices under in vitro simulated human digestion. Cereal Chem. 2017, 94, 310–314. [Google Scholar] [CrossRef]
- Balakrishnan, G.; Schneider, R.G. Quinoa flavonoids and their bioaccessibility during in vitro gastrointestinal digestion. J. Cereal Sci. 2020, 95, 103070. [Google Scholar] [CrossRef]
- Thilakarathna, S.H.; Rupasinghe, H.P.V. Flavonoid bioavailability and attempts for bioavailability enhancement. Nutrients 2013, 5, 3367–3387. [Google Scholar] [CrossRef] [PubMed]
- AACC, American Association of Cereal Chemists. AACC Official Methods 10–52, Baking Quality of Cookie Flour—Micro Method, 9th ed.; Approved Methods of the American Association of Cereal Chemists; AACC: Minneapolis, MN, USA, 1995. [Google Scholar]
- Hidalgo, A.; Brandolini, A. Heat damage of water biscuits from einkorn, durum and bread wheat flours. Food Chem. 2011, 128, 471–478. [Google Scholar] [CrossRef]
- Delgado-Andrade, C.; Conde-Aguilera, J.A.; Haro, A.; De La Cueva, S.P.; Rufián-Henares, J.A. A combined procedure to evaluate the global antioxidant response of bread. J. Cereal Sci. 2010, 56, 239–246. [Google Scholar] [CrossRef]
- Zieliński, H.; Honke, J.; Bączek, N.; Majkowska, A.; Wronkowska, M. Bioaccessibility of D-chiro-inositol from water biscuits formulated from buckwheat flours fermented by lactic acid bacteria and fungi. LWT-Food Sci. Technol. 2019, 106, 37–43. [Google Scholar] [CrossRef]
- Wiczkowski, W.; Szawara-Nowak, D.; Sawicki, T.; Mitrus, J.; Kasprzykowski, Z.; Horbowicz, M. Profile of phenolic acids and antioxidant capacity in organs of common buckwheat sprout. Acta Aliment. 2016, 45, 250–257. [Google Scholar] [CrossRef]
Figure 1.
The summed-up content of phenolic acids and flavonoids in buckwheat biscuits prepared from fermented flours by selected lactic acid bacteria.
Figure 1.
The summed-up content of phenolic acids and flavonoids in buckwheat biscuits prepared from fermented flours by selected lactic acid bacteria.
Table 1.
The content of phenolic acids (μg/g DM) in buckwheat biscuits prepared from unfermented (BBC) and fermented flours (BBF) by selected lactic acid bacteria. Data are expressed as mean ± standard deviation (n = 3). Means in each column followed by different letters are significantly different (p < 0.05) based on the one-way analysis of variance (ANOVA).
Table 1.
The content of phenolic acids (μg/g DM) in buckwheat biscuits prepared from unfermented (BBC) and fermented flours (BBF) by selected lactic acid bacteria. Data are expressed as mean ± standard deviation (n = 3). Means in each column followed by different letters are significantly different (p < 0.05) based on the one-way analysis of variance (ANOVA).
| Sample/Phenolic Acid | Vanillic | Protocatechuic | Syringic | p-Coumaric | Sinapic | t-Cinnamic | Caffeic | Ferulic |
|---|---|---|---|---|---|---|---|---|
| Control biscuits (BBc) | 112.66 ± 2.66b | 65.79 ± 2.46bc | 43.63 ± 1.33d | 21.53 ± 3.10b | 8.33 ± 0.10c | 7.86 ± 0.02d | 3.40 ± 0.11c | 3.21 ± 0.13cd |
| BBF fermented by: | ||||||||
| L. plantarum IB | 84.41 ± 3.29c | 73.48 ± 2.40b | 53.83 ± 3.03c | 16.29 ± 0.76c | 2.47 ± 0.07f | 13.15 ± 0.62ab | 3.54 ± 0.08c | 3.76 ± 0.13c |
| L. plantarum W42 | 75.60 ± 2.49d | 85.48 ± 1.96a | 50.44 ± 2.18c | 13.50 ± 3.64cd | 1.29 ± 0.05g | 14.07 ± 0.49a | 2.27 ± 0.14cd | 3.64 ± 0.11c |
| L. delbrucki subsp. bulgaricus 151 | 97.14 ± 6.39c | 52.71 ± 1.97c | 34.71 ± 0.46d | 7.58 ± 0.36e | 5.57 ± 0.24d | 2.82 ± 0.14e | 4.21 ± 0.07c | 2.47 ± 0.09e |
| L. casei Lcy | 95.40 ± 3.37c | 78.82 ± 0.98a | 36.93 ± 0.19d | 6.37 ± 0.08e | 4.76 ± 0.15e | 11.33 ± 1.01b | 3.95 ± 0.05c | 2.71 ± 0.11e |
| Streptococcus thermophilus MK-10 | 111.15 ± 4.17b | 39.72 ± 2.07d | 38.48 ± 0.66d | 8.26 ± 0.54e | 6.67 ± 0.15d | 1.87 ± 0.05e | 4.45 ± 0.11c | 2.51 ± 0.07e |
| L. acidophilus La5 | 108.18 ± 2.26b | 81.98 ± 4.05a | 46.56 ± 0.81c | 11.33 ± 0.21c | 7.77 ± 0.29cd | 3.05 ± 0.17e | 11.68 ± 0.73a | 4.29 ± 0.10b |
| L. acidophilus V | 115.33 ± 3.10b | 82.47 ± 1.00a | 60.81 ± 2.19bc | 9.67 ± 0.24d | 8.24 ± 0.15c | 4.35 ± 0.09e | 11.93 ± 1.11a | 4.17 ± 0.14bc |
| L. acidophilus 145 | 104.28 ± 0.37b | 61.19 ± 4.57c | 52.36 ± 0.55bc | 4.00 ± 0.12e | 6.20 ± 0.13d | 11.65 ± 0.50b | 2.49 ± 0.07cd | 3.23 ± 0.04c |
| L. casei 2K | 112.01 ± 1.56b | 57.00 ± 1.51c | 36.94 ± 1.53d | 12.72 ± 0.56cd | 22.35 ± 0.34a | 3.09 ± 0.02e | 10.30 ± 0.34a | 6.00 ± 0.10a |
| L. delbrucki subsp. bulgaricus K | 83.06 ± 1.59cd | 42.57 ± 0.30d | 21.42 ± 0.49e | 8.30 ± 0.35d | 4.35 ± 0.12e | 3.09 ± 0.03e | 1.59 ± 0.05d | 2.97 ± 0.11d |
| L. rhamnosus GG | 100.91 ± 0.84b | 52.52 ± 2.62c | 35.64 ± 0.96d | 13.68 ± 0.16cd | 16.24 ± 0.35b | 5.04 ± 0.35e | 7.94 ± 0.36b | 2.41 ± 0.06e |
| L. rhamnosus 8/4 | 97.22 ± 2.22c | 43.59 ± 0.50d | 45.50 ± 1.85cd | 3.41 ± 0.02e | 4.20 ± 0.04e | 5.27 ± 0.11e | 1.36 ± 0.04d | 3.44 ± 0.05c |
| L. rhamnosus K | 129.02 ± 2.65a | 73.90 ± 3.60b | 159.66 ± 6.62a | 28.53 ± 0.64a | 7.12 ± 0.38d | 10.00 ± 0.53c | 11.68 ± 0.35a | 3.19 ± 0.14cd |
| L. salivarius AWH | 95.95 ± 6.11c | 50.33 ± 1.71c | 35.30 ± 1.77d | 7.64 ± 0.32de | 8.64 ± 0.78c | 6.12 ± 0.28e | 3.17 ± 0.12c | 2.90 ± 0.12d |
| Average for BBF | 100.69 ± 14.15 | 62.55 ± 16.34 | 50.61 ± 32.98 | 10.81 ± 6.32 | 7.56 ± 5.53 | 6.78 ± 4.31 | 5.75 ± 4.04 | 3.41 ± 0.96 |
Table 2.
The content of phenolic acids (μg/g DM) in buckwheat biscuits prepared from not fermented (BBC) and fermented flours (BBF) by selected lactic acid bacteria after in vitro digestion. Data are expressed as mean ± standard deviation (n = 3). Means in each column followed by different letters are significantly different (p < 0.05) based on the one-way analysis of variance (ANOVA).
Table 2.
The content of phenolic acids (μg/g DM) in buckwheat biscuits prepared from not fermented (BBC) and fermented flours (BBF) by selected lactic acid bacteria after in vitro digestion. Data are expressed as mean ± standard deviation (n = 3). Means in each column followed by different letters are significantly different (p < 0.05) based on the one-way analysis of variance (ANOVA).
| Sample/Phenolic Acid | Vanillic | Protocatechuic | Syringic | p-Coumaric | Sinapic | t-Cinnamic | Caffeic | Ferulic |
|---|---|---|---|---|---|---|---|---|
| Control biscuits (BBc) | 187.90 ± 18.83c | 203.57 ± 6.15d | 130.65 ± 1.22c | 26.33 ± 0.14e | 22.16 ± 0.30b | 8.29 ± 0.02f | 14.64 ± 0.09e | 8.17 ± 0.21c |
| BBF fermented by: | ||||||||
| L. plantarum IB | 197.89 ± 6.37c | 327.77 ± 3.64a | 208.15 ± 6.37ab | 23.60 ± 0.19f | 24.22 ± 0.86b | 46.90 ± 0.26a | 37.38 ± 0.52c | 10.48 ± 0.18b |
| L. plantarum W42 | 243.73 ± 5.25b | 297.80 ± 7.81b | 199.22 ± 4.88ab | 26.36 ± 0.30e | 28.11 ± 0.74ab | 40.53 ± 0.95b | 52.54 ± 0.76a | 10.61 ± 0.16b |
| L. delbrucki subsp. bulgaricus 151 | 212.09 ± 5.68c | 242.62 ± 4.62d | 211.32 ± 1.23a | 28.75 ± 0.26e | 29.93 ± 0.60a | 12.41 ± 0.34f | 44.38 ± 0.48b | 10.38 ± 0.25b |
| L. casei Lcy | 226.05 ± 1.41c | 228.62 ± 2.12d | 76.55 ± 2.21d | 14.14 ± 0.24h | 6.77 ± 0.05e | 29.31 ± 0.91d | 21.98 ± 0.15d | 6.37 ± 0.09c |
| Streptococcus thermophilus MK-10 | 236.60 ± 2.85b | 166.90 ± 3.99d | 85.61 ± 1.61d | 19.59 ± 0.44g | 13.39 ± 0.26d | 17.10 ± 0.72e | 27.18 ± 0.61d | 6.95 ± 0.04c |
| L. acidophilus La5 | 233.95 ± 4.89b | 271.34 ± 9.51c | 184.67 ± 4.79b | 47.08 ± 1.25a | 32.12 ± 0.27a | 15.24 ± 0.17e | 57.05 ± 0.27a | 11.94 ± 0.14a |
| L. acidophilus V | 244.10 ± 5.66b | 285.54 ± 1.17b | 174.31 ± 4.23b | 40.18 ± 0.85b | 25.30 ± 1.04b | 17.51 ± 0.53e | 45.29 ± 1.35b | 10.44 ± 0.17b |
| L. acidophilus 145 | 247.57 ± 8.06b | 258.21 ± 6.99c | 198.11 ± 8.79ab | 17.01 ± 0.24g | 15.07 ± 0.36cd | 34.73 ± 0.21c | 23.50 ± 0.19d | 9.71 ± 0.15b |
| L. casei 2K | 233.78 ± 6.70b | 291.43 ± 3.88b | 154.45 ± 3.99c | 41.87 ± 0.45b | 30.52 ± 1.58a | 17.57 ± 0.4e | 51.27 ± 1.43a | 11.14 ± 0.29b |
| L. delbrucki subsp. bulgaricus K | 233.54 ± 1.97b | 210.31 ± 3.64d | 231.97 ± 3.90a | 27.14 ± 0.28e | 25.62 ± 0.54b | 11.59 ± 0.20f | 36.72 ± 1.31c | 10.26 ± 0.28b |
| L. rhamnosus GG | 268.28 ± 14.23a | 245.80 ± 6.36c | 177.38 ± 7.54b | 36.67 ± 0.47c | 29.11 ± 0.13a | 19.80 ± 0.67d | 49.08 ± 0.27ab | 11.01 ± 0.25b |
| L. rhamnosus 8/4 | 266.25 ± 14.04a | 339.72 ± 8.67a | 212.00 ± 8.22a | 19.29 ± 0.44g | 17.34 ± 0.08c | 19.58 ± 0.83d | 42.53 ± 0.60c | 10.43 ± 0.10b |
| L. rhamnosus K | 228.37 ± 1.05c | 265.03 ± 3.65b | 186.60 ± 6.75ab | 30.15 ± 0.29de | 30.09 ± 0.78a | 14.49 ± 0.10e | 52.30 ± 1.08a | 10.49 ± 0.18b |
| L. salivarius AWH | 281.37 ± 10.60a | 307.99 ± 2.40ab | 180.70 ± 4.93ab | 30.33 ± 0.47de | 31.22 ± 0.93a | 18.89 ± 0.49d | 46.38 ± 1.47b | 9.88 ± 0.22b |
| Average for BBF | 239.54 ± 22.01 | 267.08 ± 46.74 | 177.22 ± 45.11 | 28.73 ± 9.87 | 24.20 ± 7.91 | 22.55 ± 10.96 | 41.97 ± 11.19 | 10.01 ± 1.52 |
Table 3.
The bioaccessibility indexes (BI) of phenolic acids from buckwheat biscuits prepared from unfermented (BBC) and fermented flours (BBF) by selected lactic acid bacteria.
Table 3.
The bioaccessibility indexes (BI) of phenolic acids from buckwheat biscuits prepared from unfermented (BBC) and fermented flours (BBF) by selected lactic acid bacteria.
| Sample/Phenolic Acid | Vanillic | Protocatechuic | Syringic | p-Coumaric | Sinapic | t-Cinnamic | Caffeic | Ferulic |
|---|---|---|---|---|---|---|---|---|
| Control biscuits (BBC) | 1.67 | 3.09 | 2.99 | 1.22 | 2.66 | 1.05 | 4.31 | 2.55 |
| BBF fermented by: | ||||||||
| L. plantarum IB | 2.34 | 4.46 | 3.87 | 1.45 | 9.81 | 3.57 | 10.56 | 2.79 |
| L. plantarum W42 | 3.22 | 3.48 | 3.95 | 1.95 | 21.79 | 2.88 | 23.18 | 2.92 |
| L. delbrucki subsp. bulgaricus 151 | 2.18 | 4.60 | 6.09 | 3.79 | 5.37 | 4.40 | 10.55 | 4.20 |
| L. casei Lcy | 2.37 | 2.90 | 2.07 | 2.22 | 1.42 | 2.59 | 5.57 | 2.35 |
| Streptococcus thermophilus MK-10 | 2.13 | 4.20 | 2.22 | 2.37 | 2.01 | 9.15 | 6.11 | 2.77 |
| L. acidophilus La5 | 2.16 | 3.31 | 3.97 | 4.15 | 4.13 | 4.99 | 4.88 | 2.78 |
| L. acidophilus V | 2.12 | 3.46 | 2.87 | 4.15 | 3.07 | 4.03 | 3.80 | 2.50 |
| L. acidophilus 145 | 2.37 | 4.22 | 3.78 | 4.25 | 2.43 | 2.98 | 9.44 | 3.01 |
| L. casei 2K | 2.09 | 5.11 | 4.18 | 3.29 | 1.37 | 5.68 | 4.98 | 1.86 |
| L. delbrucki subsp. bulgaricus K | 2.81 | 4.94 | 10.83 | 3.27 | 5.89 | 3.76 | 23.12 | 3.45 |
| L. rhamnosus GG | 2.66 | 4.68 | 4.98 | 2.68 | 1.79 | 3.93 | 6.18 | 4.57 |
| L. rhamnosus 8/4 | 2.74 | 7.79 | 4.66 | 5.66 | 4.13 | 3.71 | 31.32 | 3.03 |
| L. rhamnosus K | 1.77 | 3.59 | 1.17 | 1.06 | 4.23 | 1.45 | 4.48 | 3.29 |
| L. salivarius AWH | 2.93 | 6.12 | 5.12 | 3.97 | 3.61 | 3.09 | 14.63 | 3.41 |
| Average for BBF | 2.4 ± 0.4 | 4.5 ± 1.3 | 4.3 ± 2.3 | 3.2 ± 1.3 | 5.1 ± 5.3 | 4.0 ± 1.8 | 11.3 ± 8.6 | 3.1 ± 0.7 |
Table 4.
The content of flavonoids (μg/g DM) in buckwheat biscuits prepared from not fermented (BBc) and fermented flours (BBF) by selected lactic acid bacteria. Data are expressed as mean ± standard deviation (n = 3). Means in each column followed by different letters are significantly different (p < 0.05) based on the one-way analysis of variance (ANOVA).
Table 4.
The content of flavonoids (μg/g DM) in buckwheat biscuits prepared from not fermented (BBc) and fermented flours (BBF) by selected lactic acid bacteria. Data are expressed as mean ± standard deviation (n = 3). Means in each column followed by different letters are significantly different (p < 0.05) based on the one-way analysis of variance (ANOVA).
| Strain/Flavonoid | Epicatechin | Vitexin | Orientin | Apigenin | Kaempferol | Luteolin |
|---|---|---|---|---|---|---|
| Control biscuits (BBc) | 91.69 ± 2.73c | 15.04 ± 0.21b | 4.21 ± 0.18b | 2.13 ± 0.20c | 0.75 ± 0.12b | 0.22 ± 0.02ab |
| BBF fermented by: | ||||||
| L. plantarum IB | 19.13 ± 0.33e | 7.81 ± 0.15d | 2.24 ± 0.04d | 2.91 ± 0.14b | 0.68 ± 0.05b | 0.17 ± 0.01ab |
| L. plantarum W42 | 32.50 ± 1.48d | 14.00 ± 0.11b | 2.53 ± 0.02d | 2.46 ± 0.06c | 0.89 ± 0.02b | 0.14 ± 0.01b |
| L. delbrucki subsp. bulgaricus 151 | 42.77 ± 2.15d | 14.93 ± 0.26b | 4.40 ± 0.20b | 3.41 ± 0.18a | 0.82 ± 0.07b | 0.13 ± 0.01b |
| L. casei Lcy | 41.57 ± 1.35d | 12.74 ± 0.18c | 3.10 ± 0.05cd | 2.30 ± 0.09c | 0.73 ± 0.04b | 0.12 ± 0.03b |
| Streptococcus thermophilus MK-10 | 60.54 ± 1.90d | 10.09 ± 0.23d | 3.13 ± 0.09c | 2.39 ± 0.04c | 0.52 ± 0.02c | 0.09 ± 0.01b |
| L. acidophilus La5 | 47.39 ± 4.28d | 11.77 ± 0.23c | 2.77 ± 0.10d | 1.94 ± 0.04d | 0.45 ± 0.01c | 0.12 ± 0.01b |
| L. acidophilus V | 23.20 ± 0.56e | 11.84 ± 0.33c | 3.02 ± 0.07cd | 1.99 ± 0.08d | 0.47 ± 0.05c | 0.12 ± 0.01b |
| L. acidophilus 145 | 17.92 ± 0.43e | 10.00 ± 0.13d | 3.17 ± 0.04c | 1.98 ± 0.10d | 0.45 ± 0.20c | 0.15 ± 0.02ab |
| L. casei 2K | 40.96 ± 0.84d | 11.03 ± 0.08c | 2.53 ± 0.12d | 2.63 ± 0.06c | 0.60 ± 0.16c | 0.16 ± 0.02ab |
| L. delbrucki subsp. bulgaricus K | 20.60 ± 0.49e | 9.80 ± 0.29d | 4.64 ± 0.19b | 0.67 ± 0.01e | 0.57 ± 0.02c | 0.10 ± 0.01b |
| L. rhamnosus GG | 49.87 ± 2.67d | 10.98 ± 0.28d | 2.06 ± 0.15e | 2.86 ± 0.11b | 0.57 ± 0.12c | 0.17 ± 0.03ab |
| L. rhamnosus 8/4 | 101.47 ± 6.09c | 11.61 ± 0.21c | 3.19 ± 0.09c | 2.71 ± 0.08b | 1.58 ± 0.06a | 0.22 ± 0.05ab |
| L. rhamnosus K | 114.57 ± 3.60b | 12.27 ± 0.15c | 11.48 ± 0.35a | 2.56 ± 0.09c | 0.97 ± 0.24b | 0.25 ± 0.04a |
| L. salivarius AWH | 127.64 ± 4.89a | 21.96 ± 0.64a | 3.62 ± 0.13c | 3.02 ± 0.09a | 1.07 ± 0.11b | 0.15 ± 0.05ab |
| Average for BBF | 52.87 ± 36.08 | 12.2 ± 3.33 | 3.71 ± 2.35 | 2.42 ± 0.66 | 0.74 ± 0.31 | 0.15 ± 0.04 |
Table 5.
The content of flavonoids (μg/g DM) in buckwheat biscuits prepared from not fermented (BBC) and fermented flours (BBF) by selected lactic acid bacteria after in vitro digestion. Data are expressed as mean ± standard deviation (n = 3). Means in each column followed by different letters are significantly different (p < 0.05) based on the one-way analysis of variance (ANOVA).
Table 5.
The content of flavonoids (μg/g DM) in buckwheat biscuits prepared from not fermented (BBC) and fermented flours (BBF) by selected lactic acid bacteria after in vitro digestion. Data are expressed as mean ± standard deviation (n = 3). Means in each column followed by different letters are significantly different (p < 0.05) based on the one-way analysis of variance (ANOVA).
| Strain/Flavonoid | Epicatechin | Vitexin | Orientin | Apigenin | Kaempferol | Luteolin |
|---|---|---|---|---|---|---|
| Control biscuits (BBc) | 16.45 ± 0.53d | 8.30 ± 0.29d | 4.23 ± 0.04d | 1.25 ± 0.02e | 9.27 ± 0.08a | 0.19 ± 0.02b |
| BBF fermented by: | ||||||
| L. plantarum IB | 22.35 ± 0.83d | 12.50 ± 0.08e | 6.49 ± 0.21b | 1.74 ± 0.01e | 1.99 ± 0.02d | 0.22 ± 0.02b |
| L. plantarum W42 | 42.48 ± 1.45bc | 17.51 ± 0.15b | 8.14 ± 0.20a | 2.45 ± 0.05d | 2.51 ± 0.04c | 0.24 ± 0.02b |
| L. delbrucki subsp. bulgaricus 151 | 37.27 ± 1.63c | 14.88 ± 0.50c | 6.49 ± 0.24b | 2.15 ± 0.03de | 2.06 ± 0.03cd | 0.18 ± 0.01bc |
| L. casei Lcy | 23.69 ± 1.22d | 11.65 ± 0.22e | 4.53 ± 0.15d | 1.68 ± 0.06e | 1.74 ± 0.07e | 0.15 ± 0.01c |
| Streptococcus thermophilus MK-10 | 18.12 ± 0.98d | 11.84 ± 0.10e | 6.14 ± 0.04b | 6.89 ± 0.07b | 1.40 ± 0.02e | 0.14 ± 0.03c |
| L. acidophilus La5 | 56.07 ± 0.91a | 14.08 ± 0.18c | 4.70 ± 0.02cd | 11.66 ± 0.30a | 1.83 ± 0.03d | 0.20 ± 0.01b |
| L. acidophilus V | 44.49 ± 0.89b | 14.33 ± 0.30c | 4.78 ± 0.06cd | 2.77 ± 0.07d | 1.86 ± 0.03d | 0.19 ± 0.01b |
| L. acidophilus 145 | 49.26 ± 1.57b | 17.13 ± 0.21b | 6.12 ± 0.28b | 2.94 ± 0.12d | 2.13 ± 0.03c | 0.31 ± 0.02a |
| L. casei 2K | 41.34 ± 0.98b | 19.01 ± 0.29a | 7.50 ± 0.13a | 3.15 ± 0.10d | 1.93 ± 0.03d | 0.30 ± 0.01a |
| L. delbrucki subsp. bulgaricus K | 32.93 ± 0.77c | 12.06 ± 0.15e | 4.62 ± 0.11cd | 2.26 ± 0.09e | 3.06 ± 0.04b | 0.15 ± 0.02bc |
| L. rhamnosus GG | 42.16 ± 2.44b | 12.18 ± 0.23e | 6.28 ± 0.16b | 2.82 ± 0.07d | 2.14 ± 0.02cd | 0.16 ± 0.01bc |
| L. rhamnosus 8/4 | 29.38 ± 0.89c | 13.99 ± 0.35c | 6.12 ± 0.17b | 2.09 ± 0.06e | 1.85 ± 0.03d | 0.19 ± 0.00b |
| L. rhamnosus K | 39.21 ± 1.52b | 13.40 ± 0.15d | 5.77 ± 0.06c | 2.90 ± 0.03d | 1.84 ± 0.03d | 0.20 ± 0.01b |
| L. salivarius AWH | 43.20 ± 2.22b | 12.40 ± 0.28e | 5.93 ± 0.21b | 4.25 ± 0.09c | 2.53 ± 0.06c | 0.19 ± 0.01b |
| Average for BBF | 37.28 ± 10.78 | 14.07 ± 2.24 | 5.97 ± 1.06 | 3.55 ± 2.68 | 2.06 ± 0.41 | 0.20 ± 0.05 |
Table 6.
Bioaccessibility indexes (BI) of flavonoids from buckwheat biscuits prepared from unfermented (BBC) and fermented (BBF) flours by selected lactic acid bacteria.
Table 6.
Bioaccessibility indexes (BI) of flavonoids from buckwheat biscuits prepared from unfermented (BBC) and fermented (BBF) flours by selected lactic acid bacteria.
| Strain/Flavonoid | Epicatechin | Vitexin | Orientin | Apigenin | Kaempferol | Luteolin |
|---|---|---|---|---|---|---|
| Control biscuits (BBc) | 0.18 | 0.55 | 1.01 | 0.59 | 12.29 | 0.87 |
| BBF fermented by: | ||||||
| L. plantarum IB | 1.16 | 1.60 | 2.90 | 0.60 | 2.95 | 1.27 |
| L. plantarum W42 | 1.31 | 1.25 | 3.22 | 1.00 | 2.84 | 1.71 |
| L. delbrucki subsp. bulgaricus 151 | 0.87 | 1.00 | 1.48 | 0.63 | 2.52 | 1.39 |
| L. casei Lcy | 0.57 | 0.91 | 1.46 | 0.73 | 2.38 | 1.25 |
| Streptococcus thermophilus MK-10 | 0.30 | 1.17 | 1.96 | 2.88 | 2.68 | 1.63 |
| L. acidophilus La5 | 1.18 | 1.20 | 1.69 | 6.01 | 4.03 | 1.74 |
| L. acidophilus V | 1.92 | 1.21 | 1.58 | 1.39 | 3.95 | 1.57 |
| L. acidophilus 145 | 2.75 | 1.71 | 1.93 | 1.49 | 4.68 | 2.07 |
| L. casei 2K | 1.01 | 1.72 | 2.97 | 1.20 | 3.23 | 1.93 |
| L. delbrucki subsp. bulgaricus K | 1.60 | 1.23 | 1.00 | 3.37 | 5.34 | 1.48 |
| L. rhamnosus GG | 0.85 | 1.11 | 3.05 | 0.98 | 3.74 | 0.98 |
| L. rhamnosus 8/4 | 0.29 | 1.21 | 1.92 | 0.77 | 1.17 | 0.86 |
| L. rhamnosus K | 0.34 | 1.09 | 0.50 | 1.13 | 1.89 | 0.79 |
| L. salivarius AWH | 0.34 | 0.56 | 1.64 | 1.41 | 2.37 | 1.28 |
| Average for BBF | 1.04 | 1.21 | 1.95 | 1.69 | 3.13 | 1.43 |
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Zieliński, H.; Wiczkowski, W.; Topolska, J.; Piskuła, M.K.; Wronkowska, M. Bioaccessibility of Phenolic Acids and Flavonoids from Buckwheat Biscuits Prepared from Flours Fermented by Lactic Acid Bacteria. Molecules 2022, 27, 6628. https://doi.org/10.3390/molecules27196628
AMA Style
Zieliński H, Wiczkowski W, Topolska J, Piskuła MK, Wronkowska M. Bioaccessibility of Phenolic Acids and Flavonoids from Buckwheat Biscuits Prepared from Flours Fermented by Lactic Acid Bacteria. Molecules. 2022; 27(19):6628. https://doi.org/10.3390/molecules27196628
Chicago/Turabian StyleZieliński, Henryk, Wiesław Wiczkowski, Joanna Topolska, Mariusz Konrad Piskuła, and Małgorzata Wronkowska. 2022. "Bioaccessibility of Phenolic Acids and Flavonoids from Buckwheat Biscuits Prepared from Flours Fermented by Lactic Acid Bacteria" Molecules 27, no. 19: 6628. https://doi.org/10.3390/molecules27196628
APA StyleZieliński, H., Wiczkowski, W., Topolska, J., Piskuła, M. K., & Wronkowska, M. (2022). Bioaccessibility of Phenolic Acids and Flavonoids from Buckwheat Biscuits Prepared from Flours Fermented by Lactic Acid Bacteria. Molecules, 27(19), 6628. https://doi.org/10.3390/molecules27196628
