Impact of Circular Brewer’s Spent Grain Flour after In Vitro Gastrointestinal Digestion on Human Gut Microbiota
Abstract
:1. Introduction
2. Materials and Methods
2.1. Raw Material
2.2. Extraction Procedure
2.3. Simulated In Vitro Gastrointestinal Tract
2.3.1. Oral Digestion
2.3.2. Gastric Digestion
2.3.3. Intestinal Digestion
2.3.4. Antioxidant Activity
ABTS Radical Cation Assay
Oxygen Radical Absorbance Capacity (ORAC)
Total Phenolic Content
Determination of Polyphenolic Profile and Composition
Bioaccesibility Index
2.4. Prebiotic Activity
2.5. In Vitro Fermentation Assays
2.6. Gut Microbiota Evaluation
2.6.1. DNA Extraction
2.6.2. Real-Time PCR for Microbial Analysis at Stool
2.6.3. Determination of Organic Acids
2.7. Statistical Analysis
3. Results and Discussion
3.1. Bioaccessibility under Gastrointestinal Conditions
3.1.1. Content and Profile of Phenolic Compounds
Total Phenolic Content
Individual Phenolic Compounds
3.2. Antioxidant Activity
ABTS and ORAC
3.3. Prebiotic Activity
3.4. Evolution of the Gut Microbiota Profile Groups
3.5. Organic Acids and Sugar Profiles during Gut Microbiota Fermentation
3.6. Polyphenols Profile during Gut Microbiota Fermentation
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Target Group | Maximum Growth Rate (µmax.h−1) | |||
---|---|---|---|---|
Primer Sequence (5′-3′) | Genomic DNA Standard | PCR Product Size (bp) | AT (°C) | |
Universal | AAA CTC AAA GGA ATT GAC GG ACR RCA CGA GCT GAC | Bacteroides vulgatus ATCC 8482 (DSMZ 1447) | 180 | 45 |
Firmicutes | ATG TGG TTT AAT TCG AAG CA AGC TGA CGA CAA CCA TGC AC | Lactobacillus gasseri ATCC 33,323 (DSMZ 20243) | 126 | 45 |
Enterococcus spp. | CCC TTA TTG TTA GTT GCC ATC ATT ACT CGT TGT ACT TCC CT TGT | Enterococcus gilvus ATCC BAA-350 (DSMZ 15689) | 144 | 45 |
Lacctobacillus spp. | GAG GCA GCA GTA GGG AAT CTT C GGC CAG TTA CTA CCT CTA TCC TTC TTC | Lactobacillus gasseri ATCC 33,323 (DSMZ 20243) | 126 | 55 |
Bacteroidetes | CAT GTG GTT TAA TTC GAT GAT AGC TGA CGA CAA CCA TGC AG | Bacteroides vulgatus ATCC 8482 (DSMZ 1447) | 126 | 45 |
Bacteroides spp. | ATA GCC TTT CGA AAG RAA GAT CCA GTA TCA ACT GCA ATT TTA | Bacteroides vulgatus ATCC 8482 (DSMZ 1447) | 495 | 45 |
Bifidobacterium spp. | CGC GTC YGG TGT GAA AG CCC CAC ATC CAG CAT CCA | Bifidobacterium longum subsp. Infantis ATCC 15,697 (DSMZ 20088) | 244 | 50 |
Clostridium leptum | GCA CAA GCA GTG GAG T CTT CCT CCG TTT TGT CAA | Clostridium leptum ATCC 29,065 (DSMZ 753) | 239 | 45 |
Type of Extraction mg/100g BSG | Stage | Total Phenolic Compounds (mg Gallic Acid/g BSG) | Vanillic Acid | % B | Ferulic Acid | % B | p-Coumaric Acid | % B | 4-Hydroxybenzoic Acid | % B | Catechin | % B | Vanillin | % B |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
60% ethanol:water (SLE) | Initial | 15.66 ± 2.08 A,a | 2.22 ± 0.00 A,a | - | 1.89 ± 0.06 D,a | - | 1.80 ± 0.05 B,a | - | 3.47 ± 0.08 A,a | - | 10.38 ± 0.14 A,a | - | 2.30 ± 0.01 B,a | |
Mouth | 2.77 ± 0.07 A,d | N.D. | - | 0.66 ± 0.00 C,b | 35.00 | N.D. | - | 0.92 ± 0.00 b | 26.60 | 4.38 ± 0.10 B,b | 41.18 | N.D. | ||
Stomach | 3.84 ± 0.16 C,c | N.D. | - | N.D. | - | N.D. | - | 0.06 ± 0.00 c | 1.86 | 3.68 ± 0.33 A,c | 35.50 | N.D. | ||
Intestine | 7,20 ± 0.29 B,b | N.D. | - | N.D. | - | N.D. | - | N.D. | - | 0.81 ± 0.12 A,d | 7.80 | N.D. | - | |
80% ethanol:water (SLE) | Initial | 13.77 ± 0.39 A,a | 2.06 ± 0.20 AB,a | - | 1.75 ± 0.06 C,a | - | 3.08 ± 0.05 A,a | - | 3.39 ± 0.06 AB,a | - | 8.03 ± 0.70 B,a | - | 2.45 ± 0.03 A,a | |
Mouth | 2.31 ± 0.00 B,d | N.D. | - | 0.97 ± 0.01 B,b | 55.45 | 0.28 ± 0.01 A,b | 9.09 | N.D. | - | 6.00 ± 0.34 A,b | 74.78 | N.D. | ||
Stomach | 5.74 ± 0.03 A,c | N.D. | - | N.D. | - | N.D. | - | N.D. | - | 2.08 ± 0.00 B,c | 25.93 | N.D. | ||
Intestine | 6.27 ± 0.45 D,b | N.D. | - | N.D. | - | N.D. | - | N.D. | - | 0.26 ± 0.01 C,d | 3.28 | N.D. | - | |
60% ethanol:water (OHE) | Initial | 10.91 ± 0.19 B,a | 1.85 ± 0.27 BC,a | - | 1.98 ± 0.02 B,a | - | 0.17 ± 0.02 D,b | - | 3.33 ± 0.00 B,a | - | 7.21 ± 0.51 B,a | - | 2.29 ± 0.00 B,a | |
Mouth | 2.23 ± 0.07 AB,d | N.D. | - | 0.97 ± 0.24 AB,b | 48.86 | 0.28 ± 0.00 A,a | 170.64 | N.D. | - | 1.96 ± 0.02 C,b | 27.21 | 0.97 ± 0.00 A,d | 42.57 | |
Stomach | 5.66 ± 0.09 A,c | N.D. | - | N.D. | - | N.D. | - | N.D. | - | 0.94 ± 0.01 C,c | 13.03 | 1.06 ± 0.00 B,c | 46.25 | |
Intestine | 7.39 ± 0.03 C,b | N.D. | - | N.D. | - | N.D. | - | N.D. | - | 0.29 ± 0.01 B,d | 4.06 | 1.37 ± 0.00 B,b | 59.92 | |
80% ethanol:water (OHE) | Initial | 11.51 ± 0.59 B,a | 1.62 ± 0.02 C,a | - | 2.30 ± 0.30 A,a | - | 0.92 ± 0.08 C,a | - | 3.34 ± 0.01 B,a | - | 6.62 ± 0.04 C,a | - | 2.27 ± 0.01 C,a | |
Mouth | 2.23 ± 0.03 B,d | N.D. | - | 1.08 ± 0.11 AB,b | 47.21 | 0.25 ± 0.01 B,b | 27.03 | N.D. | - | 4.26 ± 0.02 B,b | 64.37 | 0.97 ± 0.00 A,d | 42.81 | |
Stomach | 4.16 ± 0.67 B,c | N.D. | - | 0.96 ± 0.15 A,b | 88.62 | 0.22 ± 0.00 A,b | 24.11 | N.D. | - | 2.06 ± 0.02 B,c | 31.13 | 1.61 ± 0.00 A,b | 71.15 | |
Intestine | 8.36 ± 0.05 A,b | N.D. | - | N.D. | - | 0.05 ± 0.01 A,c | 5.41 | N.D. | - | 0.26 ± 0.01 C,d | 4.00 | 1.52 ± 0.00 A,c | 66.90 |
Phases of the GID | Type of Extraction | ABTS (%) | ORAC (%) | Folin-Ciocalteu (%) |
---|---|---|---|---|
Initial/Oral | 60% ethanol:water SLE | 47.04 | 81.15 | 81.04 |
80% ethanol:water SLE | 67.95 | 79.03 | 83.80 | |
60% ethanol:water OHE | 58.70 | 88.65 | 79.60 | |
80% ethanol:water OHE | 64.97 | 81.90 | 80.63 | |
Oral/Gastric | 60% ethanol:water SLE | −16.70 | −122.13 | −29.34 |
80% ethanol:water SLE | −11.50 | −63.12 | −157.46 | |
60% ethanol:water OHE | −46.58 | −348.47 | −154.47 | |
80% ethanol:water OHE | −63.46 | −193.37 | −86.58 | |
Gastric/Duodenal | 60% ethanol:water SLE | −47.30 | −102.98 | −87.46 |
80% ethanol:water SLE | −87.38 | −153.09 | −9.12 | |
60% ethanol:water OHE | −35.95 | −81.97 | −30.53 | |
80% ethanol:water OHE | −40.97 | −70.94 | −101.01 |
Division (Genus) | Number of Copies (n = 5) a |
---|---|
Universal | 7.55 ± 0.37 |
Firmicutes | 4.76 ± 0.19 |
Enterococcus spp. | 1.76 ± 0.82 |
Lactobacillus spp. | 2.93± 0.93 |
Bacteroidetes spp. | 5.05 ± 0.98 |
Bacteroides spp. | 3.73 ± 0.42 |
Bifidobacterium spp. | 4.24 ± 0.57 |
Clostridium leptum | 4.97 ± 0.25 |
F:B ratio | 0.98 ± 0.21 |
Organic Acids/Sugars (w/v) | Time (h) | Ctrl | FOS | 60% Ethanol:Water (SLE) | 80% Ethanol:Water (SLE) | 60% Ethanol:Water (OHE) | 80% Ethanol:Water (OHE) |
---|---|---|---|---|---|---|---|
Succinic acid | 0 | 0.45 ± 0.26 A,b | 0.45 ± 0.26 A,b | 0.45 ± 0.26 A,c | 0.45 ± 0.26 A,c | 0.45 ± 0.26 A,c | 0.45 ± 0.26 A,c |
12 | 1.93 ± 1.18 A,a | 1.85 ± 0.92 A,a | 1.32 ± 0.07 A,b | 1.29 ± 0.10 A,b | 1.40 ± 0.07 A,a | 1.48 ± 0.29 A,b | |
24 | 1.18 ± 0.56 B,a | 1.87 ± 0.62 B,a | 1.97 ± 0.22 B,a | 2.04 ± 0.15 B,a | 1.77 ± 0.71 AB.a | 2.07 ± 0.09 B,a | |
48 | 0.74 ± 0.71 B,b | 2.03 ± 0.85 A,a | 1.27 ± 0.08 B,b | 1.19 ± 0.09 B,b | 1.18 ± 0.06 B,b | 1.20 ± 0.04 B,b | |
Lactic acid | 0 | ND | ND | ND | ND | ND | ND |
12 | 1.21 ± 0.93 B,a | 4.04 ± 2.74 A,a | 0.23 ± 0.03 C,a | 0.25 ± 0.03 C,a | 0.28 ± 0.06 C,a | 0.30 ± 0.15 C,a | |
24 | 0.34 ± 0.14 B,b | 5.19 ± 1.40 A,a | 0.34 ± 0.04 B,a | 0.33 ± 0.06 B,a | 0.33 ± 0.09 B,a | 0.36 ± 0.14 B,a | |
48 | ND | 5.49 ± 2.14 A,a | 0.24 ± 0.06 B,a | 0.28 ± 0.11 B,a | 0.27 ± 0.04 B,a | 0.27 ± 0.06 B,a | |
Acetic acid | 0 | 0.16 ± 0.04 A,b | 0.16 ± 0.04 A,b | 0.16 ± 0.04 A,c | 0.16 ± 0.04 A,c | 0.16 ± 0.04 A,b | 0.16 ± 0.04 A,c |
12 | 0.65 ± 0.27 B,a | 1.64 ± 0.65 A,a | 0.97 ± 0.15 B,b | 0.80 ± 0.12 B,b | 0.94 ± 0.12 B,ab | 0.96 ± 0.05 B,b | |
24 | 0.74 ± 0.23 C,a | 1.48 ± 0.59 A,a | 1.12 ± 0.10 AB,ab | 1.13 ± 0.14 AB,a | 1.10 ± 0.12 BC,ab | 1.12 ± 0.11 AB,ab | |
48 | 0.69 ± 0.25 B,a | 2.29 ± 1.26 A,a | 1.22 ± 0.08 B,a | 1.24 ± 0.08 B,a | 1.38 ± 0.20 B,a | 1.30 ± 0.14 B,a | |
Propionic acid | 0 | 0.34 ± 0.09 A,c | 0.34 ± 0.09 A,b | 0.34 ± 0.09 A,c | 0.34 ± 0.09 A,b | 0.34 ± 0.09 A,c | 0.34 ± 0.09 A,c |
12 | 1.59 ± 0.32 A,a | 1.47 ± 0.60 A,a | 1.06 ± 0.36 A,b | 0.97 ± 0.61 A,a | 1.01 ± 0.13 A,b | 1.00 ± 0.41 A,b | |
24 | 0.81 ± 0.27 A,b | 1.95 ± 0.88 A,a | 1.31 ± 0.17 A,a | 1.24 ± 0.09 A,a | 1.26 ± 0.09 A,a | 1.38 ± 0.16 A,a | |
48 | 0.49 ± 0.18 C,c | 1.86 ± 0.79 A,a | 1.29 ± 0.14 AB,a | 1.23 ± 0.10 ABC,a | 1.25 ± 0.10 ABC,a | 1.22 ± 0.06 ABC,a | |
Butyric acid | 0 | 1.41 ± 0.25 A,b | 1.41 ± 0.25A,b | 1.41 ± 0.25 A,b | 1.41 ± 0.25 A,a | 1.41 ± 0.25 A,b | 1.41 ± 0.25 A,b |
12 | 1.55 ± 0.63 A,ab | 2.29 ± 0.99 A,a | 1.63 ± 0.27 A,b | 1.48 ± 0.27 A,a | 1.51 ± 0.40 A,ab | 1.54 ± 0.27 A,b | |
24 | 2.24 ± 0.67 A,a | 2.23 ± 0.66 AB,a | 2.21 ± 0.36 AB,a | 1.99 ± 0.34 B,a | 1.85 ± 0.16 B,a | 1.87 ± 0.42 B,a | |
48 | 1.83 ± 0.94 A,a | 2.70 ± 1.43 AB,a | 2.07 ± 0.18 B,a | 1.97 ± 0.62 AB,a | 2.08 ± 0.60 AB,a | 2.01 ± 0.25 AB,a | |
Total organic acids | 0 | 2.37 ± 0.64 | 2.37 ± 0.64 | 2.37 ± 0.64 | 2.37 ± 0.64 | 2.37 ± 0.64 | 2.37 ± 0.64 |
12 | 5.92 ± 3.34 | 11.29 ± 5.89 | 5.21 ± 0.78 | 4.79 ± 1.03 | 5.14 ± 0.72 | 5.18 ± 1.22 | |
24 | 5.31 ± 1.87 | 12.72 ± 4.35 | 6.95 ± 0.89 | 6.73 ± 0.79 | 6.32 ± 1.16 | 6.81 ± 0.91 | |
48 | 3.75 ± 2.08 | 14.32 ± 6.46 | 5.99 ± 0.61 | 5.82 ± 1.05 | 5.91 ± 0.98 | 5.75 ± 0.58 | |
Saccharose | 0 | 1.02 ± 0.07 A,a | 1.02 ± 0.07 A,c | 1.02 ± 0.07 A,b | 1.02 ± 0.07 A,b | 1.02 ± 0.07 A,b | 1.02 ± 0.07 A,b |
12 | 0.19 ± 0.14 D,b | 1.04 ± 0.03 C,c | 1.67 ± 0.10 B,a | 1.55 ± 0.07 B,a | 1.51 ± 0.09 B,a | 1.53 ± 0.11 Ba, | |
24 | 0.07 ± 0.01 C,c | 1.51 ± 0.09 B,a | 1.61 ± 0.12 A,a | 1.53 ± 0.05 B,a | 1.61 ± 0.07 A,a | 1.58 ± 0.11 AB,a | |
48 | 0.05 ± 0.01 C,c | 1.28 ± 0.05 A,b | 1.09 ± 0.04 B,b | 1.06 ± 0.06 B,b | 1.07 ± 0.03 B,b | 1.13 ± 0.25 AB,b | |
Glucose | 0 | 0.51 ± 0.09 A,a | 0.51 ± 0.09 A,c | 0.51 ± 0.09 A,a | 0.51 ± 0.09 A,a | 0.51 ± 0.09 A,a | 0.51 ± 0.09 A,a |
12 | 0.06 ± 0.00 C,b | 2.06 ± 0.88 A,b | 0.37 ± 0.04 B,b | 0.38 ± 0.04 B,b | 0.34 ± 0.02 B,b | 0.38 ± 0.03 B,c | |
24 | 0.06 ± 0.01 C,b | 2.51 ± 0.08 A,a | 0.49 ± 0.03 B,a | 0.45 ± 0.05 B,a | 0.47 ± 0.04 B,a | 0.43 ± 0.05 B,b | |
48 | 0.03 ± 0.01 D,c | 2.01 ± 0.09 A,b | 0.34 ± 0.06 B,b | 0.19 ± 0.05 C,c | 0.31 ± 0.07 BC,b | 0.17 ± 0.05 C,d |
Type of Extraction (mg/100 g BSG) | Stage | Vanillic Acid | Ferulic Acid | 4-Hydroxybenzoic Acid | Catechin | p-Coumaric | Vanillin |
---|---|---|---|---|---|---|---|
60% ethanol:water (SLE) | 0 | N.D. | N.D. | N.D. | N.D. | N.D. | N.D. |
12 | 1.36 ± 0.75 A,a | 3.01 ± 0.51 A,a | 1.98 ± 0.02 A,b | 21.07 ± 1.61 AB,a | N.D. | N.D. | |
24 | 1.03 ± 0.58 A,a | 1.03 ± 0.44 A,c | 6.14 ± 1.16 A,a | 17.57 ± 2.51 ab | N.D. | N.D. | |
48 | 0.82 ± 0.46 A,a | 2.28 ± 0.35 A,b | 0.82 ± 0.34 A,c | 12.31 ± 3.64 b | N.D. | N.D. | |
80% ethanol:water (SLE) | 0 | N.D. | N.D. | N.D. | N.D. | N.D. | N.D. |
12 | 1.50 ± 0.81 A,a | 2.43 ± 0.19 AB,a | 1.88 ± 0.26 A,b | 16.61 ± 2.80 B,a | N.D. | N.D. | |
24 | 1.20 ± 0.68 A,a | 0.93 ± 0.32 A,b | 6.01 ± 1.37 A,a | 19.93 ± 4.01 a | N.D. | N.D. | |
48 | 0.75 ± 0.41 A,a | 2.44 ± 0.28 A,a | 1.39 ± 1.17 A,b | 14.89 ± 4.97 a | N.D. | N.D. | |
60% ethanol:water (OHE) | 0 | N.D. | N.D. | N.D. | N.D. | N.D. | N.D. |
12 | 1.43 ± 0.78 A,a | 2.29 ± 0.22 AB,a | 1.80 ± 0.26 A,b | 23.72 ± 3.27 AB,a | N.D. | 1.72 ± 1.40 A,a | |
24 | 1.06 ± 0.61 A,a | 1.00 ± 0.45 A,b | 8.00 ± 1.27 A,a | 18.66 ± 2.27 ab | N.D. | 0.14 ± 0.08 A,b | |
48 | 0.91 ± 0.57 A,a | 2.17 ± 0.45 AB,a | 0.89 ± 0.37 A,b | 13.52 ± 4.90 b | N.D. | N.D. | |
80% ethanol:water (OHE) | 0 | N.D. | N.D. | N.D. | N.D. | N.D. | N.D. |
12 | 1.44 ± 0.77 A,a | 2.14 ± 0.21 B,a | 1.88 ± 0.54 A,b | 16.26 ± 5.39 B,a | 0.27 ± 0.13 A,a | 2.20 ± 0.78 A,a | |
24 | 1.03 ± 0.57 A,a | 1.07 ± 0.35 A,c | 7.68 ± 0.92 A,a | 22.01 ± 4.91 a | N.D. | 0.18 ± 0.07 A,b | |
48 | 0.91 ± 0.50 A,a | 1.60 ± 0.14 B,b | 0.67 ± 0.14 A,c | 11.23 ± 1.53 b | N.D. | N.D. |
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Bonifácio-Lopes, T.; Catarino, M.D.; Vilas-Boas, A.A.; Ribeiro, T.B.; Campos, D.A.; Teixeira, J.A.; Pintado, M. Impact of Circular Brewer’s Spent Grain Flour after In Vitro Gastrointestinal Digestion on Human Gut Microbiota. Foods 2022, 11, 2279. https://doi.org/10.3390/foods11152279
Bonifácio-Lopes T, Catarino MD, Vilas-Boas AA, Ribeiro TB, Campos DA, Teixeira JA, Pintado M. Impact of Circular Brewer’s Spent Grain Flour after In Vitro Gastrointestinal Digestion on Human Gut Microbiota. Foods. 2022; 11(15):2279. https://doi.org/10.3390/foods11152279
Chicago/Turabian StyleBonifácio-Lopes, Teresa, Marcelo D. Catarino, Ana A. Vilas-Boas, Tânia B. Ribeiro, Débora A. Campos, José A. Teixeira, and Manuela Pintado. 2022. "Impact of Circular Brewer’s Spent Grain Flour after In Vitro Gastrointestinal Digestion on Human Gut Microbiota" Foods 11, no. 15: 2279. https://doi.org/10.3390/foods11152279