Fig Leaves (Ficus carica L.): Source of Bioactive Ingredients for Industrial Valorization
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals, Reagents, and Samples
2.2. Samples Preparation
2.3. Color Measurement
2.4. Preparation of Hydroethanolic Extracts
2.5. Chromatographic Analysis of Chemical Constituents
2.5.1. Organic Acids
2.5.2. Free Sugars
2.5.3. Tocopherols
2.5.4. Fatty Acids
2.5.5. Phenolic Compounds
2.6. Evaluation of Bioactive Properties
2.6.1. Antioxidant Activity
2.6.2. Cytotoxic and Hepatotoxic Activities
2.6.3. Inhibition of Nitric Oxide Production Evaluation
2.6.4. Antimicrobial Activity
2.7. Statistical Analysis
3. Results and Discussion
3.1. Color Measurement
3.2. Chemical Composition
3.2.1. Organic Acids
3.2.2. Free Sugars
3.2.3. Tocopherols
3.2.4. Fatty Acids
3.2.5. Phenolic Compounds
3.3. Bioactivity Evaluation
3.3.1. Antioxidant Activity
3.3.2. Cytotoxic Activities
3.3.3. Inhibition of Nitric Oxide Production Evaluation
4. Antimicrobial Activity
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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PA | LA | DA | BN | MA | |
---|---|---|---|---|---|
CIELAB | |||||
L* | 35.0 ± 0.3 c | 38.2 ± 0.8 b | 36.8 ± 0.5 b | 41.1 ± 0.6 a | 37.1 ± 0.3 b |
a* | −7.1 ± 0.7 b | −11.0 ± 0.4 a | −7.7 ± 0.7 b | −7.7 ± 0.8 b | −7.3 ± 0.3 b |
b* | 11.1 ± 0.4 b | 16.1 ± 0.9 a | 12.0 ± 0.6 b | 17.7 ± 0.4 a | 12.6 ± 0.4 b |
Color |
Organic Acids (g/100 g dw) | |||||
---|---|---|---|---|---|
PA | LA | DA | BN | MA | |
▊ Oxalic | 41.6 ± 0.6 c | 60.0 ± 0.6 a | 11.90 ± 0.08 d | 48.8 ± 0.2 b | 41.0 ± 0.7 c |
▊ Quinic | 16.1 ± 0.2 c | 19.03 ± 0.08 b | 23.0 ± 0.2 a | 23.3 ± 0.2 a | 19.5 ± 0.6 b |
▊ Malic | 40.1 ± 0.4 c | 2.54 ± 0.03 d | 55.8 ± 0.2 a | 52.5 ± 0.6 b | 55.49 ± 0.6 a |
▊ Citric | 22.4 ± 0.3 d | 23.1 ± 0.2 c | 27.6 ± 0.4 a | 21.8 ± 0.4 e | 24.1 ± 0.1 b |
▊ Shikimic | tr | nd | nd | 0.11 ± 0.06 | nd |
Ascorbic | nd | tr | nd | tr | tr |
Fumaric | tr | tr | tr | tr | tr |
Total | 120.2 ± 0.7 c | 104.7 ± 0.8 d | 118.3 ± 0.4 c | 146.5 ± 1.1 a | 140.1 ± 0.3 b |
Free Sugars (g/100 g dw) | |||||
---|---|---|---|---|---|
PA | LA | DA | BN | MA | |
▊ Fructose | 1.36 ± 0.02 e | 1.94 ± 0.02 c | 7.34 ± 0.06 a | 3.58 ± 0.02 b | 1.75 ± 0.01 d |
▊ Glucose | 1.48 ± 0.02 e | 1.77 ± 0.02 d | 7.72 ± 0.04 a | 6.32 ± 0.007 b | 3.59 ± 0.02 c |
▊ Sucrose | 1.62 ± 0.01 c | 0.133 ± 0.007 e | 0.276 ± 0.008 d | 4.27 ± 0.03 a | 3.59 ± 0.01 b |
▊ Trehalose | 0.62 ± 0.02 c | 0.63 ± 0.01 c | 1.130 ± 0.009 a | 0.61 ± 0.01 c | 0.72 ± 0.01 b |
▊ Raffinose | 0.26 ± 0.01 e | 0.47 ± 0.02 d | 0.87 ± 0.01 a | 0.74 ± 0.01 b | 0.687 ± 0.008 c |
Total | 5.34 ± 0.02 d | 4.95 ± 0.02 e | 17.36 ± 0.08 a | 15.57 ± 0.03 b | 10.08 ± 0.06 c |
Tocopherols (mg/100 g dw) | |||||
---|---|---|---|---|---|
PA | LA | DA | BN | MA | |
▊ α-Tocoferol | 3.36 ± 0.05 a | 3.32 ± 0.05 a | 2.26 ± 0.02 b | 1.438 ± 0.004 c | 1.45 ± 0.01 c |
▊ β-Tocoferol | 0.29 ± 0.01 a | 0.23 ± 0.02 b | 0.14 ± 0.01 c | 0.21 ± 0.01 b | 0.142 ± 0.008 c |
▊ γ-Tocoferol | 0.49 ± 0.01 a | nd | 0.51 ± 0.02 a | 0.188 ± 0.007 c | 0.26 ± 0.01 b |
▊ δ-Tocoferol | nd | nd | nd | nd | nd |
Total | 4.14 ± 0.04 a | 3.56 ± 0.06 b | 2.91 ± 0.03 c | 1.84 ± 0.01 d | 1.85 ± 0.01 d |
Fatty Acids (% of Total) | |||||
---|---|---|---|---|---|
PA | LA | DA | BN | MA | |
C12:0 | nd | 0.911 ± 0.004 | nd | nd | nd |
C13:0 | nd | 2.171 ± 0.008 b | 1.65 ± 0.02 d | 2.87 ± 0.15 a | 1.77 ± 0.06 c |
C14:0 | nd | 3.11 ± 0.02 a | 1.39 ± 0.04 d | 2.30 ± 0.04 b | 1.87 ± 0.01 c |
C14:1 | nd | nd | 0.316 ± 0.004 | nd | nd |
C15:1 | nd | nd | 0.346 ± 0.003 | nd | nd |
C16:0 | 18.9 ± 0.4 b | 23.19 ± 0.07 a | 19.05 ± 0.05 b | 18.1 ± 0.3 c | 16.5 ± 0.1 d |
C16:1 | nd | nd | 1.457 ± 0.002 | nd | 1.66 ± 0.03 |
C17:0 | nd | nd | 0.756 ± 0.001 | nd | nd |
C18:0 | 7.8 ± 0.2 a | nd | 4.77 ± 0.02 d | 6.5 ± 0.2 b | 5.26 ± 0.02 c |
C18:1n9c | nd | nd | 4.62 ± 0.04 a | nd | 3.941 ± 0.006 b |
C18:2n6c | 13.5 ± 0.5 c | 19.68 ± 0.05 a | 12.25 ± 0.09 d | 15.27 ± 0.02 b | 10.318 ± 0.004 e |
C18:3n3 | 52.9 ± 0.2 a | 44.23 ± 0.02 b | 40.334 ± 0.001 c | 36.8 ± 0.3 e | 38.99 ± 0.02 d |
C20:0 | nd | nd | 3.41 ± 0.02 b | nd | 4.63 ± 0.05 a |
C20:3n3 | nd | 6.71 ± 0.07 b | 1.420 ± 0.001 d | 18.4 ± 0.2 a | 3.6 ± 0.1 c |
C22:0 | 6.7 ± 0.2 a | nd | 4.045 ± 0.006 c | nd | 6.26 ± 0.02 b |
C24:0 | nd | nd | 4.19 ± 0.04 | nd | 5.3 ± 0.1 |
▊ SFA | 33.4 ± 0.3 c | 29.4 ± 0.1 d | 39.3 ± 0.1 b | 29.7 ± 0.2 d | 41.5 ± 0.09 a |
▊ MUFA | nd | nd | 6.73 ± 0.03 | nd | 5.60 ± 0.03 |
▊ PUFA | 66.4 ± 0.2 b | 70.6 ± 0.1 a | 54.00 ± 0.09 c | 70.5 ± 0.1 a | 52.9 ± 0.1 d |
Quantification (mg/g dw Extract) | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|
Peak | Rt (min) | λmax (nm) | [M−H]− (m/z) | MS2 (m/z) | TentativeIdentification | PA | LA | DA | BN | MA |
1 | 5.99 | 320 | 341 | 179 (100), 161 (18), 135 (5) | Caffeic acid hexoside | 0.747 ± 0.007 b | 0.56 ± 0.02 c | 1.08 ± 0.02 a | 0.427 ± 0.006 d | 0.54 ± 0.01 c |
2 | 7.08 | 324 | 353 | 191 (100), 179 (12), 161 (7), 135 (5) | cis 5-O-caffeoylquinic acid | 1.52 ± 0.04 a | 1.22 ± 0.02 b | 1.27 ± 0.05 b | 0.548 ± 0.007 d | 0.67 ± 0.02 c |
3 | 7.26 | 324 | 353 | 191 (100), 179 (9), 161 (8), 135 (5) | trans 5-O-Caffeoylquinic acid | nd | nd | 2.361 ± 0.003 | nd | nd |
4 | 10.12 | 328 | 579 | 459 (22), 429 (83), 357 (63), 327 (100), 309 (54) | Luteolin O-pentosyl-C-hexoside | 3.5 ± 0.1 c | 7.7 ± 0.1 a | 3.99 ± 0.07 b | 0.092 ± 0.001 e | 3.1 ± 0.1 d |
5 | 10.54 | 324 | 179 | 163 (100) | Caffeic acid | 2.55 ± 0.03 b | 3.68 ± 0.03 a | 2.16 ± 0.05 c | 0.71 ± 0.01 e | 1.02 ± 0.03 d |
6 | 11.7 | 283 | 337 | 191 (100), 163 (12), 119 (10) | 5-O-p-Coumaroylquinic acid | 3.624 ± 0.002 a | 0.95 ± 0.03 b | 0.92 ± 0.02 b | 0.599 ± 0.001 d | 0.68 ± 0.02 c |
7 | 12.88 | 337 | 563 | 473 (58), 443 (100), 383 (15), 353 (20), 311 (5), 297 (5) | Apigenin-C-hexoside-C-pentoside | 6.63 ± 0.04 c | 13.62 ± 0.08 a | 8.83 ± 0.09 b | 6.19 ± 0.06 e | 6.40 ± 0.02 d |
8 | 14.37 | 338 | 563 | 473 (58), 443 (100), 383 (15), 353 (20), 311 (5), 297 (5) | Apigenin-C-hexoside-C-pentoside | 0.562 ± 0.002 d | 0.87 ± 0.02 b | 1.01 ± 0.01 a | 0.592 ± 0.009 c | 0.60 ± 0.01 c |
9 | 15.72 | 287 | 545 | 501 (100), 459 (13), 313 (5), 167 (98) | Vanilic acid -malonyl-rhamnoside-rhamnoside | 0.104 ± 0.001 d | 0.238 ± 0.003 a | 0.181 ± 0.001 b | 0.175 ± 0.001 c | 0.178 ± 0.003 b,c |
10 | 16.82 | 355 | 609 | 301 (100) | Quercetin-O-deoxyhexosyl-hexoside | 6.72 ± 0.03 c | 9.33 ± 0.03 b | 9.903 ± 0.005 a | 5.293 ± 0.004 e | 5.97 ± 0.02 d |
11 | 18.21 | 351 | 463 | 301 (100) | Quercetin-O-hexoside | 1.426 ± 0.005 b | 1.00 ± 0.02 c | 1.16 ± 0.02 a | 0.586 ± 0.003 e | 0.668 ± 0.002 d |
12 | 19.58 | 355 | 549 | 505 (52), 463 (43), 301 (100) | Quercetin-O-malonyl-hexoside | 3.640 ± 0.005 a | 1.90 ± 0.03 b | 1.39 ± 0.02 c | 0.826 ± 0.001 e | 1.28 ± 0.0 d |
13 | 20 | 359 | 593 | 285 (100) | Kaempherol-O-deoxyhexosyl-hexoside | 0.895 ± 0.009 c | 1.38 ± 0.02 a | 1.05 ± 0.01 b | 0.718 ± 0.006 d | 0.735 ± 0.009 d |
▊Total Phenolic Acids | 8.54 ± 0.02 a | 6.6 ± 0.1 c | 7.98 ± 0.05 b | 2.455 ± 0.002 e | 3.08 ± 0.03 d | |||||
▊Total Flavonoids | 23.4 ± 0.1 c | 35.80 ± 0.08 a | 27.3 ± 0.1 b | 14.30 ± 0.04 e | 18.7 ± 0.2 d | |||||
Total Phenolic Compounds | 31.9 ± 0.1 c | 42.4 ± 0.2 a | 35.3 ± 0.2 b | 16.75 ± 0.04 e | 21.8 ± 0.2 d |
PA | LA | DA | BN | MA | Positive Control | ||
---|---|---|---|---|---|---|---|
Antioxidant Activity | |||||||
TBARS (EC50, mg/mL) | 0.78 ± 0.02 d | 0.74 ± 0.02 d | 0.35 ± 0.01 b | 0.23 ± 0.01 a | 0.45 ± 0.03 c | 0.0091 ± 0.0003 | |
CAA (% inhibition by 2 mg/mL) | 65 ± 11 a | 60 ± 4 a | 57 ± 5 a | 40 ± 3 b | 33 ± 3 c | 95 ± 5 | |
Cytotoxic activity | |||||||
AGS | (GI50, µg/mL) | >400 | 173 ± 12 b | 158 ± 13 a | 235 ± 23 c | >400 | 1.23 ± 0.03 |
MCF-7 | 253 ± 12 b,c | 208 ± 7 a | 223 ± 2 a,b | >400 | 279 ± 24 c | 1.02 ± 0.02 | |
CaCo2 | >400 | >400 | >400 | >400 | >400 | 1.21 ± 0.02 | |
VERO | >400 | >400 | >400 | >400 | >400 | 1.41 ± 0.06 | |
PLP2 | >400 | 225 ± 1 a | 248 ± 10 b | >400 | >400 | 1.4 ± 0.1 | |
Inhibition of nitric oxide production evaluation | |||||||
NO production inhibition (IC50, µg/mL) | 82 ± 8 b | >400 | 20 ± 5 a | >400 | 89 ± 3 b | 6.3 ± 0.4 |
Fig Leaves Varieties | Positive Control | |||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
PA | LA | DA | BN | MA | Streptomycin (1 mg/mL) | Methicillin (1 mg/mL) | Ampicillin (20 mg/mL) | |||||||||
MIC | MBC | MIC | MBC | MIC | MBC | MIC | MBC | MIC | MBC | MIC | MBC | MIC | MBS | MIC | MBC | |
Gram-negative bacteria | ||||||||||||||||
E. cloacae | 10 | >10 | 10 | >10 | 10 | >10 | 10 | >10 | 10 | >10 | 0.007 | 0.007 | n.t. | n.t | 0.15 | 0.15 |
E. coli | 10 | >10 | 10 | >10 | 2.5 | >10 | 5 | >10 | 5 | >10 | 0.01 | 0.01 | n.t. | n.t. | 0.15 | 0.15 |
P. aeruginosa | >10 | >10 | >10 | >10 | >10 | >10 | >10 | >10 | >10 | >10 | 0.06 | 0.06 | n.t. | n.t. | 0.63 | 0.63 |
S. enterica | 10 | >10 | 10 | >10 | 5 | >10 | 10 | >10 | 10 | >10 | 0.007 | 0.007 | n.t. | n.t. | 0.15 | 0.15 |
Y. enterocolitica | 10 | >10 | 5 | >10 | 1.25 | >10 | 0.6 | >10 | 0.6 | >10 | 0.007 | 0.007 | n.t. | n.t. | 0.15 | 0.15 |
Gram-positive bacteria | ||||||||||||||||
B. cereus | 10 | >10 | 10 | >10 | >10 | >10 | >10 | >10 | >10 | >10 | 0.007 | 0.007 | n.t. | n.t. | n.t. | n.t. |
L. monocytogenes | 5 | >10 | >10 | >10 | >10 | >10 | >10 | >10 | >10 | >10 | 0.007 | 0.007 | n.t. | n.t. | 0.15 | 0.15 |
S. aureus | 10 | >10 | 10 | >10 | 2.5 | >10 | 10 | >10 | 10 | >10 | 0.007 | 0.007 | 0.007 | 0.007 | 0.15 | 0.15 |
Fungal strains | Ketaconazole (1 mg/mL) | |||||||||||||||
MIC | MFC | MIC | MFC | MIC | MFC | MIC | MFC | MIC | MFC | MIC | MFC | |||||
A. brasiliensis | 10 | >10 | 10 | >10 | 10 | >10 | 10 | >10 | 10 | >10 | 0.06 | 0.125 | ||||
A. fumigatus | 5 | >10 | 10 | >10 | >10 | >10 | 10 | >10 | 10 | >10 | 0.5 | 1 |
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Shiraishi, C.S.H.; Zbiss, Y.; Roriz, C.L.; Dias, M.I.; Prieto, M.A.; Calhelha, R.C.; Alves, M.J.; Heleno, S.A.; V., d.C.M.; Carocho, M.; et al. Fig Leaves (Ficus carica L.): Source of Bioactive Ingredients for Industrial Valorization. Processes 2023, 11, 1179. https://doi.org/10.3390/pr11041179
Shiraishi CSH, Zbiss Y, Roriz CL, Dias MI, Prieto MA, Calhelha RC, Alves MJ, Heleno SA, V. dCM, Carocho M, et al. Fig Leaves (Ficus carica L.): Source of Bioactive Ingredients for Industrial Valorization. Processes. 2023; 11(4):1179. https://doi.org/10.3390/pr11041179
Chicago/Turabian StyleShiraishi, Carlos S. H., Yosra Zbiss, Custódio Lobo Roriz, Maria Inês Dias, Miguel A. Prieto, Ricardo C. Calhelha, Maria José Alves, Sandrina A. Heleno, da Cunha Mendes V., Márcio Carocho, and et al. 2023. "Fig Leaves (Ficus carica L.): Source of Bioactive Ingredients for Industrial Valorization" Processes 11, no. 4: 1179. https://doi.org/10.3390/pr11041179