By-Products of Camu-Camu [Myrciaria dubia (Kunth) McVaugh] as Promising Sources of Bioactive High Added-Value Food Ingredients: Functionalization of Yogurts
Abstract
:1. Introduction
2. Results and Discussion
2.1. Phenolic Compounds Profiles
2.2. Evaluation of Bioactive Properties
2.3. Fortification of Yogurt with Camu-Camu Peel Extract
3. Materials and Methods
3.1. Preparation of the Camu-Camu Extracts
3.2. Phenolic Compounds Analysis
3.3. Antimicrobial Activity
3.4. Anti-Proliferative Activity and Hepatotoxicity
3.5. Fortification of Yogurt with Camu-Camu Peel Extract
3.6. Nutritional Parameters
3.7. pH and Phenolic Compounds Evaluation
3.8. Statistical Analysis
4. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Sample Availability: Samples of the fruits and compounds are not available from the authors. |
Peak | Rt (min) | λmax (nm) | [M − H]−/[M]+ m/z | Main MS2 Fragments (m/z) | Tentative Identification | Reference | Concentration (mg/g Extract) |
---|---|---|---|---|---|---|---|
Peel | |||||||
Non-anthocyanins | |||||||
1 | 6.0 | 324 | 353 | 191(22),179(45),173(100),161(10),135(5) | 4-O-Caffeoylquinic acid | [21] | 1.41 ± 0.04 |
2 | 7.2 | 314 | 325 | 163(100) | p-Coumaroyl hexoside | [3] | 2.71 ± 0.02 |
3 | 14.9 | 255,356 | 417 | 255(100) | (Iso)liquiritigenin-O-hexoside | [22] | 1.38 ± 0.02 |
4 | 15.1 | 255,356 | 417 | 255(100) | (Iso)liquiritigenin-O-hexoside | [22] | 0.71 ± 0.01 |
5 | 16.1 | 257,352 | 417 | 255(100) | (Iso)liquiritigenin-O-hexoside | [22] | 0.323 ± 0.003 |
6 | 17.2 | 256,354 | 449 | 312(100) | Myricetin-O-pentoside | [1] | 4.91 ± 0.08 |
7 | 17.4 | 350 | 463 | 317(100) | Myricetin-O-deoxyhexoside | [1] | 2.47 ± 0.01 |
8 | 21.4 | 335 | 431 | 269(100) | Apigenin-O-hexoside | [3] | 4.1 ± 0.2 |
9 | 27.5 | 360 | 719 | 301(100) | Ellagic acid derivative | [1] | 1.56 ± 0.01 |
10 | 28.0 | 360 | 719 | 301(100) | Ellagic acid derivative | [1] | 1.43 ± 0.01 |
11 | 30.8 | 362 | 733 | 301(100) | Ellagic acid derivative | - | 2.17 ± 0.04 |
12 | 31.0 | 360 | 733 | 301(100) | Ellagic acid derivative | - | 2.61 ± 0.03 |
Anthocyanins | |||||||
13 | 15.7 | 523 | 465 | 303(100) | Delphinidin-3-O-glucoside | [23] | 2.98 ± 0.04 |
14 | 19.2 | 515 | 449 | 287(100) | Cyanindin-3-O-glucoside | [23] | 4.68 ± 0.07 |
TPC | 33.4 ± 0.5 | ||||||
Pulp | |||||||
Non-anthocyanins | |||||||
2 | 7.0 | 344 | 325 | 163(100) | p-Coumaroyl hexoside | [3] | 1.77 ± 0.01 |
15 | 8.2 | 326 | 355 | 193(100) | Ferulic acid hexoside | [3] | 0.307 ± 0.002 |
16 | 14.3 | 350 | 479 | 317(100) | Myricetin-O-hexoside | [1] | 0.613 ± 0.003 |
6 | 17.0 | 352 | 449 | 317(100) | Myricetin-O-pentoside | [1] | 0.63 ± 0.01 |
Anthocyanins | |||||||
14 | 19.0 | 515 | 449 | 287(100) | Cyanidin-3-O-glucoside | [23] | 1.000 ± 0.001 |
TPC | 4.32 ± 0.03 | ||||||
Seed | |||||||
Non-anthocyanins | |||||||
17 | 5.0 | 242,370 | 469 | 425(100),407(22),300(10) | Valoneic acid dilactone | [1] | 1.893 ± 0.004 |
18 | 6.5 | 243,272 | 935 | 917(24),633(100),301(12) | Di-HHDP-galloyl-glucoside | [1] | 1.41 ± 0.01 |
19 | 12.9 | 243,360 | 463 | 301(100) | Ellagic acid hexoside | [1] | 2.12 ± 0.01 |
4 | 15.0 | 271,360 | 417 | 250(100) | (Iso)liquiritigenin-O-hexoside | [22] | tr |
20 | 16.9 | 246,360 | 433 | 301(100) | Ellagic acid pentoside | [1] | 5.59 ± 0.03 |
21 | 18.5 | 252,365 | 301 | 284(10),245(3),185(4),173(5),157(3),145(6) | Ellagic acid | [1] | 8.57 ± 0.03 |
22 | 24.4 | 250,361 | 489 | 301(100) | Ellagic acetyl rhamnoside | [1] | 2.07 ± 0.01 |
23 | 25.3 | 252,361 | 489 | 301(100) | Ellagic acetyl rhamnoside | [1] | 1.75 ± 0.01 |
TPC | 23.41 ± 0.07 |
Peel | Pulp | Seed | Ampicillin (20 mg/mL) | Imipenem (1 mg/mL) | Vancomycin (1 mg/mL) | Fluconazole (1 mg/mL) | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Antibacterial activity | MIC | MBC | MIC | MBC | MIC | MBC | MIC | MBC | MIC | MBC | MIC | MBC | MIC | MFC |
Gram-negative bacteria | ||||||||||||||
Escherichia coli | 10 | >20 | 10 | >20 | 20 | >20 | <0.15 | <0.15 | <0.0078 | <0.0078 | nt | nt | nt | nt |
Klebsiella pneumoniae | 10 | >20 | 20 | >20 | 20 | >20 | 10 | 20 | <0.0078 | <0.0078 | nt | nt | nt | nt |
Morganella morganii | 2.5 | >20 | 5 | >20 | 20 | >20 | 20 | >20 | <0.0078 | <0.0078 | nt | nt | nt | nt |
Proteus mirabilis | 10 | 20 | 10 | >20 | 10 | >20 | <0.15 | <0.15 | <0.0078 | <0.0078 | nt | nt | nt | nt |
Pseudomonas aeruginosa | 5 | >20 | 10 | >20 | 10 | >20 | >20 | >20 | 0.5 | 1 | nt | nt | nt | nt |
Gram-positive bacteria | ||||||||||||||
Enterococcus faecalis | 10 | >20 | 10 | >20 | 20 | >20 | <0.15 | <0.15 | nt | nt | <0.0078 | <0.0078 | nt | nt |
Listeria monocytogenes | 5 | >20 | >20 | >20 | 2.5 | >20 | <0.15 | <0.15 | <0.0078 | <0.0078 | nt | nt | nt | nt |
MRSA | 0.625 | >20 | 10 | >20 | 20 | >20 | <0.15 | <0.15 | nt | nt | <0.0078 | <0.0078 | nt | nt |
MSSA | 0.625 | >20 | 10 | >20 | 10 | >20 | <0.15 | <0.15 | nt | nt | 0.25 | 0.5 | nt | nt |
Antifungal activity | ||||||||||||||
Candida albicans | 20 | >20 | >20 | >20 | 10 | >20 | nt | nt | nt | nt | nt | nt | 0.06 | 0.06 |
Camu-camu | Peel | Pulp | Seed | p-Student t-Test |
---|---|---|---|---|
Anti-proliferative activity (GI50, µg/mL) 1 | ||||
HepG2 (hepatocellular carcinoma) | 238 ± 10 | 297 ± 15 | >400 | 0.001 |
NCI-H460 (non-small cell lung cancer) | 304 ± 12 | >400 | >400 | - |
HeLa (cervical carcinoma) | 180 ± 8 c | 196 ± 7 b | 320 ± 1 a | - |
MCF-7 (breast carcinoma) | 279 ± 15 | 331 ± 15 | >400 | 0.004 |
Hepatotoxicity (GI50, µg/mL) 1 | ||||
PLP2 | >400 | >400 | >400 | - |
Nutritional Parameters | |||||||||
---|---|---|---|---|---|---|---|---|---|
Storage Time | Sample | Moisture | Fat | Protein | Carbohydrates | Ash | Energy | Galactose | Lactose |
0 days | Control | 84.4 ± 0.1 | 3.78 ± 0.02 | 5.8 ± 0.1 | 5.12 ± 0.08 | 0.95 ± 0.03 | 77.6 ± 0.2 | 1.035 ± 0.006 | 2.531 ± 0.003 |
Fortified | 84.4 ± 0.8 | 3.68 ± 0.08 | 5.90 ± 0.09 | 5.1 ± 0.1 | 0.887 ± 0.003 | 77.2 ± 0.3 | 1.042 ± 0.009 | 2.57 ± 0.03 | |
p-Student t-Test | 0.031 | 0.036 | 0.114 | 0.999 | 0.005 | 0.087 | 0.181 | 0.048 | |
7 days | Control | 82.4 ± 0.6 | 4.18 ± 0.07 | 6.5 ± 0.1 | 6.0 ± 0.1 | 0.97 ± 0.01 | 87.6 ± 0.3 | 1.13 ± 0.04 | 2.8 ± 0.1 |
Fortified | 83.1 ± 0.3 | 4.02 ± 0.05 | 6.39 ± 0.09 | 5.63 ± 0.08 | 0.86 ± 0.03 | 84.3 ± 0.2 | 1.13 ± 0.01 | 2.81 ± 0.06 | |
p-Student t-Test | 0.001 | 0.011 | 0.145 | 0.002 | 0.001 | <0.001 | 0.785 | 0.356 | |
15 days | Control | 81.6 ± 0.7 | 4.49 ± 0.03 | 6.8 ± 0.1 | 6.1 ± 0.1 | 1.01 ± 0.04 | 91.9 ± 0.2 | 1.22 ± 0.04 | 3.03 ± 0.04 |
Fortified | 82.8 ± 0.4 | 4.16 ± 0.02 | 6.5 ± 0.1 | 5.53 ± 0.02 | 1.02 ± 0.04 | 85.68 ± 0.05 | 1.15 ± 0.04 | 2.850 ± 0.005 | |
p-Student t-Test | <0.001 | <0.001 | 0.019 | 0.001 | 0.702 | <0.001 | 0.034 | <0.001 |
Storage Time | |||||||||
---|---|---|---|---|---|---|---|---|---|
0 days | 7 days | 15 days | |||||||
Control | Fortified | p-Student´s t-Test | Control | Fortified | p-Student´s t-Test | Control | Fortified | p-Student´s t-Test | |
C4:0 | 5.02 ± .02 | 6.29 ± 0.01 | <0.0001 | 4.186 ± 0.003 | 3.359 ± 0.008 | <0.001 | 3.39 ± 0.07 | 3.293 ± 0.001 | 0.034 |
C6:0 | 3.379 ± 0.001 | 4.81 ± 0.07 | <0.0001 | 3.10 ± 0.02 | 3.14 ± 0.02 | 0.034 | 3.138 ± 0.001 | 2.960 ± 0.005 | <0.001 |
C8:0 | 1.78 ± 0.01 | 2.41 ± 0.02 | <0.0001 | 1.596 ± 0.004 | 1.709 ± 0.008 | <0.001 | 1.68 ± 0.02 | 1.628 ± 0.001 | 0.002 |
C10:0 | 3.465 ± 0.008 | 4.33 ± 0.01 | <0.0001 | 3.215 ± 0.001 | 3.238 ± 0.006 | 0.001 | 3.427 ± 0.014 | 3.34 ± 0.01 | <0.001 |
C11:0 | 0.094 ± 0.008 | 0.099 ± 0.009 | 0.367 | 0.098 ± 0.001 | 0.077 ± 0.001 | <0.001 | 0.082 ± 0.007 | 0.084 ± 0.006 | 0.617 |
C12:0 | 3.635 ± 0.04 | 4.10 ± 0.03 | <0.0001 | 3.534 ± 0.001 | 3.412 ± 0.008 | <0.001 | 3.74 ± 0.01 | 3.698 ± 0.003 | 0.001 |
C13:0 | 0.103 ± 0.001 | 0.111 ± 0.001 | <0.0001 | 0.113 ± 0.004 | 0.087 ± 0.003 | <0.001 | 0.102 ± 0.001 | 0.105 ± 0.001 | 0.007 |
C14:0 | 11.42 ± 0.05 | 11.217 ± 0.01 | <0.0001 | 11.42 ± 0.02 | 11.00 ± 0.03 | <0.001 | 11.87 ± 0.02 | 11.97 ± 0.01 | <0.001 |
C14:1 | 1.17 ± 0.01 | 1.145 ± 0.008 | 0.013 | 1.17 ± 0.01 | 1.09 ± 0.03 | 0.003 | 1.20 ± 0.03 | 1.20 ± 0.01 | 0.877 |
C15:0 | 1.286 ± 0.007 | 1.20 ± 0.02 | 0.001 | 1.292 ± 0.009 | 1.279 ± 0.006 | 0.047 | 1.323 ± 0.008 | 1.351 ± 0.001 | 0.001 |
C15:1 | 0.271 ± 0.008 | 0.25 ± 0.01 | 0.004 | 0.263 ± 0.001 | 0.263 ± 0.005 | 0.824 | 0.272 ± 0.008 | 0.275 ± 0.001 | 0.435 |
C16:0 | 32.21 ± 0.06 | 30.35 ± 0.07 | <0.0001 | 33.239 ± 0.004 | 33.22 ± 0.06 | 0.452 | 33.33 ± 0.06 | 33.778 ± 0.008 | <0.001 |
C16:1 | 1.365 ± 0.004 | 1.27 ± 0.01 | <0.0001 | 1.391 ± 0.001 | 1.352 ± 0.006 | <0.001 | 1.370 ± 0.005 | 1.393 ± 0.009 | 0.006 |
C17:0 | 0.608 ± 0.002 | 0.57 ± 0.02 | 0.006 | 0.630 ± 0.005 | 0.641 ± 0.004 | 0.011 | 0.624 ± 0.002 | 0.629 ± 0.001 | 0.006 |
C17:1 | 0.243 ± 0.001 | 0.22 ± 0.01 | 0.005 | 0.246 ± 0.001 | 0.254 ± 0.001 | <0.001 | 0.241 ± 0.006 | 0.25 ± 0.002 | 0.026 |
C18:0 | 9.66 ± 0.02 | 9.726 ± 0.007 | 0.002 | 10.132 ± 0.003 | 10.473 ± 0.001 | <0.001 | 9.824 ± 0.006 | 9.872 ± 0.006 | <0.001 |
C18:1n9 | 19.72 ± 0.02 | 17.2 ± 0.2 | <0.0001 | 20.12 ± 0.02 | 20.64 ± 0.03 | <0.001 | 19.60 ± 0.05 | 19.737 ± 0.004 | 0.002 |
C18:2n6 | 2.13 ± 0.05 | 2.13 ± 0.03 | 0.844 | 2.083 ± 0.001 | 2.33 ± 0.08 | 0.002 | 2.28 ± 0.05 | 2.21 ± 0.02 | 0.029 |
C18:3n3 | 1.672 ± 0.001 | 1.57 ± 0.02 | <0.0001 | 1.460 ± 0.001 | 1.654 ± 0.004 | <0.001 | 1.59 ± 0.01 | 1.578 ± 0.009 | 0.226 |
C20:0 | 0.133 ± 0.004 | 0.145 ± 0.001 | 0.003 | 0.17 ± 0.02 | 0.126 ± 0.006 | 0.004 | 0.142 ± 0.001 | 0.149 ± 0.001 | <0.001 |
C20:1 | 0.04 ± 0.01 | 0.043 ± 0.001 | 0.016 | 0.039 ± 0.001 | 0.041 ± 0.001 | 0.001 | 0.039 ± 0.001 | 0.039 ± 0.001 | 0.999 |
C20:3n6 | 0.16 ± 0.01 | 0.199 ± 0.006 | 0.003 | 0.236 ± 0.003 | 0.13 ± 0.01 | <0.001 | 0.314 ± 0.001 | 0.14 ± 0.01 | <0.001 |
C20:4n6 | 0.200 ± 0.001 | 0.32 ± 0.02 | <0.0001 | 0.171 ± 0.001 | 0.24 ± 0.02 | 0.001 | 0.26 ± 0.01 | 0.174 ± 0.004 | <0.001 |
C20:3n3 | 0.16 ± 0.01 | 0.138 ± 0.008 | 0.028 | 0.006 ± 0.001 | 0.13 ± 0.02 | <0.001 | 0.077 ± 0.002 | 0.058 ± 0.006 | 0.002 |
C22:0 | 0.084 ± 0.01 | 0.128 ± 0.001 | <0.0001 | 0.112 ± 0.002 | 0.11 ± 0.02 | 0.852 | 0.106 ± 0.003 | 0.099 ± 0.001 | 0.003 |
SFA | 72.87 ± 0.07 | 75.5 ± 0.2 | <0.0001 | 72.82 ± 0.01 | 71.87 ± 0.04 | <0.001 | 72.76 ± 0.01 | 72.96 ± 0.04 | <0.001 |
MUFA | 22.812 ± 0.003 | 20.2 ± 0.2 | <0.0001 | 23.220 ± 0.007 | 23.65 ± 0.04 | <0.001 | 22.72 ± 0.06 | 22.895 ± 0.006 | 0.003 |
PUFA | 4.32 ± 0.07 | 4.36 ± 0.03 | 0.274 | 3.955 ± 0.004 | 4.49 ± 0.08 | <0.001 | 4.51 ± 0.05 | 4.15 ± 0.03 | <0.001 |
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Conceição, N.; Albuquerque, B.R.; Pereira, C.; Corrêa, R.C.G.; Lopes, C.B.; Calhelha, R.C.; Alves, M.J.; Barros, L.; C. F. R. Ferreira, I. By-Products of Camu-Camu [Myrciaria dubia (Kunth) McVaugh] as Promising Sources of Bioactive High Added-Value Food Ingredients: Functionalization of Yogurts. Molecules 2020, 25, 70. https://doi.org/10.3390/molecules25010070
Conceição N, Albuquerque BR, Pereira C, Corrêa RCG, Lopes CB, Calhelha RC, Alves MJ, Barros L, C. F. R. Ferreira I. By-Products of Camu-Camu [Myrciaria dubia (Kunth) McVaugh] as Promising Sources of Bioactive High Added-Value Food Ingredients: Functionalization of Yogurts. Molecules. 2020; 25(1):70. https://doi.org/10.3390/molecules25010070
Chicago/Turabian StyleConceição, Natália, Bianca R. Albuquerque, Carla Pereira, Rúbia C. G. Corrêa, Camila B. Lopes, Ricardo C. Calhelha, Maria José Alves, Lillian Barros, and Isabel C. F. R. Ferreira. 2020. "By-Products of Camu-Camu [Myrciaria dubia (Kunth) McVaugh] as Promising Sources of Bioactive High Added-Value Food Ingredients: Functionalization of Yogurts" Molecules 25, no. 1: 70. https://doi.org/10.3390/molecules25010070