Optimization and Bioactive Evaluation of Bifurcaria bifurcata Antioxidant-Rich Extracts for Functional Food and Pharmaceutical Applications
Abstract
:1. Introduction
2. Materials and Methods
2.1. Material and Reagents
2.2. Algae Collection and Preparation
2.3. Microwave-Assisted Extraction
2.4. Experimental Design, Modeling, and Optimization
2.5. Model Independent Variables
2.5.1. Yield
2.5.2. Total Polyphenol Content (TPC)
2.5.3. DPPH• Scavenging Activity
Experimental Design | Responses | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Coded Values | Natural Values | ||||||||||
X1 | X2 | X3 | X1: t | X2: P | X3:S | Y | TPC | DPPH• | ABTS | BCM | |
min | Bar | % | mg/g dw | mg FE/g dw | nM R·/g dw | nM R·/g dw | µM βC/g dw | ||||
1 | −1 | −1 | −1 | 7.5 | 5.6 | 20.3 | 426.77 | 57.12 | 32.70 | 41.73 | 0.0902 |
2 | −1 | −1 | 1 | 7.5 | 5.6 | 79.7 | 330.76 | 46.50 | 32.12 | 159.51 | 0.1037 |
3 | −1 | 1 | −1 | 7.5 | 16.4 | 20.3 | 514.74 | 69.46 | 39.99 | 44.61 | 0.1060 |
4 | −1 | 1 | 1 | 7.5 | 16.4 | 79.7 | 362.82 | 52.28 | 34.79 | 280.31 | 0.0354 |
5 | 1 | −1 | −1 | 20.5 | 5.6 | 20.3 | 541.44 | 61.89 | 42.05 | 53.86 | 0.1279 |
6 | 1 | −1 | 1 | 20.5 | 5.6 | 79.7 | 370.05 | 52.19 | 29.83 | 56.22 | 0.0481 |
7 | 1 | 1 | −1 | 20.5 | 16.4 | 20.3 | 462.27 | 61.70 | 41.84 | 29.30 | 0.0913 |
8 | 1 | 1 | 1 | 20.5 | 16.4 | 79.7 | 326.94 | 48.42 | 26.19 | 184.17 | 0.0712 |
9 | 1.68 | 0 | 0 | 25 | 11 | 50 | 423.36 | 58.72 | 32.49 | 168.26 | 0.0806 |
10 | −1.68 | 0 | 0 | 3 | 11 | 50 | 339.81 | 64.29 | 44.94 | 165.00 | 0.0870 |
11 | 0 | −1.68 | 0 | 14 | 2 | 50 | 323.71 | 44.04 | 30.59 | 84.13 | 0.0950 |
12 | 0 | 1.68 | 0 | 14 | 20 | 50 | 457.90 | 63.23 | 38.15 | 85.67 | 0.0757 |
13 | 0 | 0 | −1.68 | 14 | 11 | 0 | 452.43 | 43.58 | 26.07 | 180.96 | 0.0959 |
14 | 0 | 0 | 1.68 | 14 | 11 | 100 | 100.33 | 19.23 | 13.25 | 22.51 | 0.0017 |
15 | −1.68 | −1.68 | −1.68 | 3 | 2 | 0 | 283.57 | 24.48 | 12.20 | 216.08 | 0.0677 |
16 | −1.68 | −1.68 | 1.68 | 3 | 2 | 100 | 59.64 | 6.07 | 2.22 | 4.46 | 0.0017 |
17 | −1.68 | 1.68 | −1.68 | 3 | 20 | 0 | 393.25 | 33.17 | 17.52 | 18.40 | 0.0781 |
18 | −1.68 | 1.68 | 1.68 | 3 | 20 | 100 | 115.62 | 16.39 | 11.76 | 19.92 | 0.0046 |
19 | 1.68 | −1.68 | −1.68 | 25 | 2 | 0 | 345.64 | 31.39 | 16.46 | 181.43 | 0.1029 |
20 | 1.68 | −1.68 | 1.68 | 25 | 2 | 100 | 55.48 | 2.93 | 1.46 | 2.70 | 0.0017 |
21 | 1.68 | 1.68 | −1.68 | 25 | 20 | 0 | 365.07 | 32.35 | 17.77 | 36.29 | 0.0391 |
22 | 1.68 | 1.68 | 1.68 | 25 | 20 | 100 | 112.57 | 11.38 | 14.17 | 36.33 | 0.0096 |
23 | 0 | 0 | 0 | 14 | 11 | 50 | 385.65 | 62.49 | 33.79 | 169.41 | 0.0946 |
24 | 0 | 0 | 0 | 14 | 11 | 50 | 371.11 | 69.10 | 32.96 | 195.22 | 0.0950 |
25 | 0 | 0 | 0 | 14 | 11 | 50 | 411.94 | 62.68 | 27.71 | 199.82 | 0.0908 |
26 | 0 | 0 | 0 | 14 | 11 | 50 | 369.34 | 62.99 | 30.63 | 119.88 | 0.0926 |
27 | 0 | 0 | 0 | 14 | 11 | 50 | 400.93 | 59.00 | 23.27 | 180.36 | 0.1029 |
28 | 0 | 0 | 0 | 14 | 11 | 50 | 380.33 | 48.41 | 23.03 | 183.10 | 0.0959 |
2.5.4. Azino-Bis(3-Ethylbenzothiazoline-6-Sulfonic Acid) ABTS•+ Scavenging Activity
2.5.5. β-Carotene Discoloration Method (BCM)
2.6. Mathematical Model
2.7. Numerical Methods, Statistical Analysis, and Figures
2.8. Biological Activities Assessment at the Optimal BB Extract
2.8.1. Antimicrobial Assay
2.8.2. ROS and RNS Scavenging Activity
2.8.3. Enzyme Inhibition Assays
2.8.4. Cell Line Studies
Anti-Inflammatory Activity
Cytotoxicity Activity Assay
3. Results and Discussion
3.1. Mathematical Modelling of the Optimization
Coefficients | Parametric Responses to the CCCD | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Extract | Chemical | Antioxidant Activity | |||||||||
Yield | TPC | DPPH• | ABTS•+ | BCM | |||||||
(A) FITTING COEFFICIENTS OBTAINED | |||||||||||
Intercept | b0 | 408.105 | ±17.983 | 61.645 | ±2.237 | 28.649 | ±2.473 | 170.106 | ±14.562 | 0.095 | ±0.006 |
Linear effect | b1 | ns | −0.385 | ±0.131 | ns | −43.670 | ±23.646 | ns | |||
b2 | 17.384 | ±10.519 | 2.597 | ±1.309 | 1.857 | ±1.006 | 61.489 | ±23.646 | −0.005 | ±0.003 | |
b3 | −80.007 | ±10.519 | −6.451 | ±1.309 | −3.113 | ±1.006 | 121.825 | ±23.646 | −0.021 | ±0.003 | |
Quadratic effect | b11 | ns | ns | 4.563 | ±1.636 | ns | ns | ||||
b22 | ns | ns | 3.026 | ±1.636 | −33.331 | ±11.353 | ns | ||||
b33 | −28.218 | ±16.798 | −8.872 | ±2.090 | −2.174 | ±1.636 | −28.079 | ±11.353 | −0.019 | ±0.003 | |
Cubic effect | b111 | ns | ns | ns | 15.440 | ±9.306 | ns | ||||
b22 | ns | ns | ns | −30.280 | ±9.306 | ns | |||||
b333 | ns | ns | ns | −55.446 | ±9.306 | ns | |||||
Interactive effect | b12 | ns | ns | ns | ns | ns | |||||
b13 | ns | ns | ns | ns | ns | ||||||
b23 | ns | ns | ns | 14.363 | ±5.008 | ns | |||||
b123 | ns | ns | ns | ns | 0.003 | ±0.001 | |||||
b1122 | ns | ns | ns | ns | ns | ||||||
b1133 | ns | ns | ns | ns | ns | ||||||
b2233 | ns | ns | ns | ns | ns | ||||||
b112233 | −4.865 | ±2.022 | −0.734 | ±0.252 | −1.422 | ±0.332 | 2.760 | ±1.839 | ns | ||
R2 | 0.8916 | 0.9290 | 0.8792 | 0.8871 | 0.8608 | ||||||
(B) OPTIMAL CONDITIONS AND RESPONSE VALUES | |||||||||||
Optimum conditions | X1: t (min) | 14.00 | ±1.87 | 3.00 | ±0.87 | 3.00 | ±0.87 | 7.57 | ±1.38 | 25.00 | ±2.50 |
X2: P (bar) | 20.00 | ±2.24 | 20.00 | ±2.24 | 20.00 | ±2.24 | 14.25 | ±1.89 | 2.00 | ±0.71 | |
X3: S (%) | 7.85 | ±1.40 | 43.49 | ±3.30 | 46.58 | ±3.41 | 71.94 | ±4.24 | 26.04 | ±2.55 | |
Responses | mg/g dw | mg/g dw | nM R•/g dw | nM R•/g dw | µM βC/g dw | ||||||
494.05 | ±54.64 | 67.37 | ±18.47 | 53.42 | ±11.72 | 275.94 | ±14.48 | 0.11 | ±1.48 |
3.2. Influence of Extraction Conditions on Response Variables
3.3. Biological Activity of the BB Optimal Extract
3.3.1. Antimicrobial Activity
A: Antimicrobial activity | |||
MIC (mg/mL) | Inhibition zone (mm) | ||
Escherichia coli | NI | NI | Lactic acid 40% (18.96 ± 3.59) |
Staphylococcus epidermidis | 8 | 15.86 ± 1.43 | Lactic acid 40% (17.43 ± 3.41) |
Bacillus cereus | 1.2 | 5.45 ± 1.06 | Lactic acid 40% (17.10 ± 3.36) |
Staphylococcus aureus | >8 | 12.06 ± 1.88 | Lactic acid 40% (19.08 ± 4.59) |
Salmonella enteritidis | 1.2 | 9.77 ± 1.63 | Lactic acid 40% (18.06 ± 2.93) |
Pseudomonas aeruginosa | >8 | 10.86 ± 0.23 | Lactic acid 40% (19.45 ± 1.45) |
B:Antioxidant activity (ROS, RNS) | |||
IC50 (µg/mL) | IC50 (µg/mL) | ||
Hydroxyl radical (●OH) | 446.1 ± 22.3 | Ascorbic acid (183 µg/mL) | |
Nitric oxide (●NO) | 55.35 ±2.76 | Ascorbic acid (446 µg/mL) | |
Superoxide anion (O2●–) | 44.25 ± 2.21 | Ascorbic acid (160 µg/mL) | |
Hydrogen peroxide (H2O2) | 108.4 ± 5.4 | Ascorbic acid (51 µg/mL) | |
C:Enzymatic inhibition | |||
IC50 (µg/mL) | IC50 (µg/mL) | ||
Tyrosinase | 329.6 ± 16.4 | Kojic acid (1.82 µg/mL) | |
Monoamine oxidase A (MAO-A) | 133.6 ± 6.68 | Clorgyline (25 ng/mL) | |
Monoamine oxidase B (MAO-B) | 154.8 ± 7.74 | Selegiline (2.1 µg/mL) | |
Acetylcholinesterase (AChE) | >2000 | Galantamine (0.92 µg/mL) | |
Butyrylcholinesterase (BuChE) | 712.9 ± 35 | Galantamine (4.92 µg/mL) | |
D: Anti-inflammatory activity | |||
IC50 (µg/mL) | IC50 (µg/mL) | ||
RAW264.7 | 320.5 ± 10.6 | Dexamethasone 7.23 ± 0.85 | |
E: Cytotoxic effects | |||
IC50 (µg/mL) | IC50 (µg/mL) | ||
A549 (lung adenocarcinoma) | 87.57 ± 2.04 | Ellipticine (<1 mg/mL) | |
HEPG2 (hepatocellular carcinoma) | 52.85 ± 2.71 | Ellipticine (0.85 ± 0.046) | |
AGS (gastric adenocarcinoma) | 38.75 ± 2.18 | Ellipticine (<1 mg/mL) | |
Vero | 85.85 ± 2.67 | Ellipticine (<1 mg/mL) |
3.3.2. Reactive Oxygen and Nitrogen Scavenging Activity
3.3.3. In Vitro Neuroprotective Properties
3.3.4. Anti-Inflammatory and Cytotoxic Properties
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Silva, A.; Carpena, M.; Cassani, L.; Grosso, C.; Garcia-Oliveira, P.; Delerue-Matos, C.; Simal-Gandara, J.; Barroso, M.F.; Prieto, M.A. Optimization and Bioactive Evaluation of Bifurcaria bifurcata Antioxidant-Rich Extracts for Functional Food and Pharmaceutical Applications. Antioxidants 2024, 13, 1189. https://doi.org/10.3390/antiox13101189
Silva A, Carpena M, Cassani L, Grosso C, Garcia-Oliveira P, Delerue-Matos C, Simal-Gandara J, Barroso MF, Prieto MA. Optimization and Bioactive Evaluation of Bifurcaria bifurcata Antioxidant-Rich Extracts for Functional Food and Pharmaceutical Applications. Antioxidants. 2024; 13(10):1189. https://doi.org/10.3390/antiox13101189
Chicago/Turabian StyleSilva, Aurora, Maria Carpena, Lucia Cassani, Clara Grosso, Paula Garcia-Oliveira, Cristina Delerue-Matos, Jesus Simal-Gandara, Maria Fatima Barroso, and Miguel A. Prieto. 2024. "Optimization and Bioactive Evaluation of Bifurcaria bifurcata Antioxidant-Rich Extracts for Functional Food and Pharmaceutical Applications" Antioxidants 13, no. 10: 1189. https://doi.org/10.3390/antiox13101189