The Application of Ultrasonic Waves and Microwaves to Improve Antihyperglycaemic and Antimicrobial Activities of Marrubium vulgare Extracts
Abstract
:1. Introduction
2. Results and Discussion
2.1. Extraction Yield
2.2. Total Phenolic Content
2.3. Total Flavonoid Content
2.4. Antioxidant Activity
2.5. Model Fitting
2.6. Process Parameters Influencing UAE and MAE
2.7. Phenolic Acids
2.8. Process Optimization
2.9. Antihyperglycaemic Activity
2.10. Antimicrobial Activity
3. Materials and Methods
3.1. Plant Material
3.2. Chemicals
3.3. Conventional Solid/Liquid Extraction
3.4. Ultrasound-Assisted Extraction (UAE)
3.5. Microwave-Assisted Extraction (MAE)
3.6. Analysis of Bioactive Compounds
3.6.1. Total Phenols Content
3.6.2. Total Flavonoids Content
3.6.3. DPPH Assay
3.6.4. FRAP Assay
3.6.5. HPLC Analyses of Phenolic Acids
3.7. Antihyperglycaemic Activity
3.7.1. α-Amylase Inhibitory Potential (α-AIP)
3.7.2. α-Glucosidase Inhibitory Potential (α-GIP)
3.8. Antimicrobial Activity
3.9. Design of Experiments
4. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Independent Variables | Investigated Responses | |||||||
---|---|---|---|---|---|---|---|---|
Run Order | Temperature (°C) | Extraction Time (min) | Ultrasonic Power (W/L) | Y (mg/mL) | TP (mg GAE/g) | TF (mg CE/g) | IC50 (mg/mL) | EC50 (mg/mL) |
1 | 60 | 60 | 42 | 15.92 | 85.10 | 50.42 | 0.0172 | 0.0593 |
2 | 60 | 40 | 60 | 16.02 | 87.66 | 52.40 | 0.0180 | 0.0566 |
3 | 80 | 40 | 42 | 18.48 | 99.30 | 53.19 | 0.0218 | 0.0575 |
4 | 60 | 60 | 42 | 15.76 | 76.36 | 49.84 | 0.0178 | 0.0591 |
5 | 60 | 80 | 60 | 17.42 | 80.10 | 48.58 | 0.0177 | 0.0576 |
6 | 40 | 80 | 42 | 15.16 | 78.94 | 44.97 | 0.0215 | 0.0561 |
7 | 80 | 60 | 60 | 20.08 | 92.39 | 50.93 | 0.0256 | 0.0636 |
8 | 40 | 40 | 42 | 12.91 | 76.00 | 49.03 | 0.0199 | 0.0480 |
9 | 60 | 60 | 42 | 16.90 | 82.45 | 44.67 | 0.0178 | 0.0557 |
10 | 40 | 60 | 60 | 15.35 | 73.66 | 49.08 | 0.0207 | 0.0505 |
11 | 60 | 60 | 42 | 15.95 | 82.15 | 51.10 | 0.0164 | 0.0562 |
12 | 60 | 40 | 24 | 15.19 | 79.85 | 50.51 | 0.0170 | 0.0524 |
13 | 80 | 60 | 24 | 17.95 | 94.57 | 44.59 | 0.0193 | 0.0566 |
14 | 60 | 80 | 24 | 17.15 | 77.58 | 49.15 | 0.0222 | 0.0569 |
15 | 40 | 60 | 24 | 13.61 | 83.89 | 50.35 | 0.0197 | 0.0427 |
16 | 80 | 80 | 42 | 19.11 | 90.00 | 48.25 | 0.0217 | 0.0568 |
17 | 60 | 60 | 42 | 16.22 | 86.99 | 52.97 | 0.0218 | 0.0606 |
Independent Variables | Investigated Responses | |||||||
---|---|---|---|---|---|---|---|---|
Run Order | Extraction Time (min) | Ethanol Conc. (%) | Microwave Power (W) | Y (mg/mL) | TP (mg GAE/g) | TF (mg CE/g) | IC50 (mg/mL) | EC50 (mg/mL) |
1 | 35 | 50 | 400 | 18.29 | 107.08 | 56.05 | 0.0216 | 0.0671 |
2 | 15 | 50 | 400 | 18.20 | 106.85 | 57.97 | 0.0197 | 0.0635 |
3 | 15 | 70 | 600 | 13.74 | 102.58 | 65.54 | 0.0192 | 0.0475 |
4 | 25 | 30 | 400 | 18.26 | 93.33 | 59.58 | 0.0188 | 0.0630 |
5 | 15 | 50 | 800 | 18.70 | 86.05 | 54.70 | 0.0171 | 0.0636 |
6 | 25 | 50 | 600 | 17.26 | 92.89 | 57.92 | 0.0198 | 0.0659 |
7 | 35 | 50 | 800 | 20.36 | 81.94 | 52.10 | 0.0275 | 0.0651 |
8 | 25 | 50 | 600 | 19.07 | 109.13 | 52.42 | 0.0159 | 0.0726 |
9 | 25 | 50 | 600 | 19.65 | 82.28 | 49.98 | 0.0212 | 0.0677 |
10 | 25 | 70 | 800 | 16.36 | 94.00 | 57.30 | 0.0240 | 0.0590 |
11 | 25 | 30 | 800 | 22.30 | 94.36 | 49.76 | 0.0164 | 0.0776 |
12 | 35 | 30 | 600 | 22.61 | 86.69 | 53.46 | 0.0129 | 0.0790 |
13 | 25 | 50 | 600 | 18.95 | 89.36 | 52.96 | 0.0186 | 0.0657 |
14 | 25 | 70 | 400 | 14.64 | 96.04 | 62.78 | 0.0195 | 0.0528 |
15 | 15 | 30 | 600 | 20.69 | 82.29 | 50.93 | 0.0178 | 0.0735 |
16 | 35 | 70 | 600 | 14.33 | 117.58 | 65.80 | 0.0259 | 0.0445 |
17 | 25 | 50 | 600 | 18.16 | 116.94 | 54.58 | 0.0175 | 0.0633 |
Ultrasound Assisted Extraction | Microwave Assisted Extraction | ||
---|---|---|---|
Extraction Yield | |||
p-value | p-value | ||
Model | 0.0002 * | Model | 0.0054 * |
X1-Temperature | <0.0001 * | X1-Extraction time | 0.2208 |
X2-Extraction time | 0.0034 * | X2-Ethanol concentration | 0.0001 * |
X3-Ultrasonic power | 0.0105 ** | X3-Microwave power | 0.0339 ** |
X1 × X2 | 0.1566 | X1 × X2 | 0.5696 |
X1 × X3 | 0.7143 | X1 × X3 | 0.5051 |
X2 × X3 | 0.5972 | X2 × X3 | 0.3367 |
X12 | 0.2930 | X12 | 0.8479 |
X22 | 0.9427 | X22 | 0.1481 |
X32 | 0.2470 | X32 | 0.7798 |
Lack of fit | 0.3136 | Lack of fit | 0.2446 |
Total phenols content | |||
p-value | p-value | ||
Model | 0.0423 ** | Model | 0.0024 * |
X1-Temperature | 0.0013 * | X1-Extraction time | 0.6941 |
X2-Extraction time | 0.2320 | X2-Ethanol concentration | 0.0008 * |
X3-Ultrasonic power | 0.8710 | X3-Microwave power | 0.0006 * |
X1 × X2 | 0.2040 | X1 × X2 | 0.9955 |
X1 × X3 | 0.3880 | X1 × X3 | 0.6239 |
X2 × X3 | 0.5638 | X2 × X3 | 0.4306 |
X12 | 0.0931 *** | X12 | 0.0238 ** |
X22 | 0.7544 | X22 | 0.0246 ** |
X32 | 0.7782 | X32 | 0.0137 ** |
Lack of fit | 0.3594 | Lack of fit | 0.0692 *** |
Total flavonoids content | |||
p-value | p-value | ||
Model | 0.0195 ** | Model | 0.0396 ** |
X1-Temperature | 0.6171 | X1-Extraction time | 0.8377 |
X2-Extraction time | 0.0123 ** | X2-Ethanol concentration | 0.0024 * |
X3-Ultrasonic power | 0.1637 | X3-Microwave power | 0.0281 ** |
X1 × X2 | 0.2324 | X1 × X2 | 0.7070 |
X1 × X3 | 0.0047 * | X1 × X3 | 0.9099 |
X2 × X3 | 0.2107 | X2 × X3 | 0.4765 |
X12 | 0.0145 ** | X12 | 0.4200 |
X22 | 0.6597 | X22 | 0.0485 ** |
X32 | 0.1588 | X32 | 0.7988 |
Lack of fit | 0.4961 | Lack of fit | 0.0590 *** |
IC50 value | |||
p-value | p-value | ||
Model | 0.0006 * | Model | 0.0432 ** |
X1-Temperature | 0.1235 | X1-Extraction time | 0.0605 *** |
X2-Extraction time | 0.2852 | X2-Ethanol concentration | 0.0091 * |
X3-Ultrasonic power | 0.0512 *** | X3-Microwave power | 0.4196 |
X1 × X2 | 0.2903 | X1 × X2 | 0.0367 ** |
X1 × X3 | 0.0029 * | X1 × X3 | 0.1003 |
X2 × X3 | 0.0054 * | X2 × X3 | 0.1696 |
X12 | <0.0001 * | X12 | 0.3658 |
X22 | 0.1935 | X22 | 0.5369 |
X32 | 0.0421 ** | X32 | 0.1437 |
Lack of fit | 0.2875 | Lack of fit | 0.3580 |
EC50 value | |||
p-value | p-value | ||
Model | 0.0458 ** | Model | 0.0460 ** |
X1-Temperature | 0.0037 * | X1-Extraction time | 0.6595 |
X2-Extraction time | 0.1828 | X2-Ethanol concentration | 0.0010 * |
X3-Ultrasonic power | 0.0559 *** | X3-Microwave power | 0.2885 |
X1 × X2 | 0.1967 | X1 × X2 | 0.4941 |
X1 × X3 | 0.8936 | X1 × X3 | 0.8581 |
X2 × X3 | 0.5826 | X2 × X3 | 0.4932 |
X12 | 0.0792 *** | X12 | 0.4893 |
X22 | 0.7284 | X22 | 0.2220 |
X32 | 0.2764 | X32 | 0.9648 |
Lack of fit | 0.1248 | Lack of fit | 0.0708 *** |
Sample | Content (μg/mL) | ||||||
---|---|---|---|---|---|---|---|
Ferulic Acid | p-Coumaric Acid | Caffeic Acid | Rutin | Hyperoside | Chlorogenic Acid | Quercetin | |
96% EtOH | 5.05 | 6.67 | 6.43 | 20.41 | 2.71 | n.d. | n.d. |
70% EtOH | 21.38 | 23.89 | 13.86 | 190.43 | 13.05 | n.d. | n.d. |
50% EtOH (MAC) | 35.86 | 30.60 | 18.10 | 236.93 | 25.58 | n.d. | n.d. |
30% EtOH | 25.02 | 29.49 | 35.26 | 87.51 | 11.39 | n.d. | n.d. |
MAC-W | 8.39 | tr | tr | 30.63 | 5.78 | n.d. | n.d. |
UAEopt | 1.34 | 4.75 | 0.26 | 49.59 | 19.06 | 33.11 | 34.88 |
MAEopt | 1.07 | 4.26 | tr | 34.01 | 14.71 | 23.23 | 30.05 |
Extraction Method | Optimized Conditions | Predicted Responses | Observed Responses |
---|---|---|---|
UAE | Y = 16.93% | Y = 16.90% | |
Temperature: 73.6 °C | TP = 91.48 mg GAE/g | TP = 109.62 mg GAE/g | |
Extraction time: 40 min | TF = 50.07 mg CE/g | TF = 53.36 mg CE/g | |
Ultrasonic power: 30.3 W/L | IC50 = 0.0181 mg/mL | IC50 = 0.0189 mg/mL | |
EC50 = 0.0564 mg/mL | EC50 = 0.0623 mg/mL | ||
MAE | Y = 15.76% | Y = 16.66% | |
Ethanol concentration: 63.8% | TP = 110.04 mg GAE/g | TP = 110.26 mg GAE/g | |
Extraction time: 15 min | TF = 62.45 mg CE/g | TF = 54.86 mg CE/g | |
Microwave power: 422 W | IC50 = 0.0191 mg/mL | IC50 = 0.0180 mg/mL | |
EC50 = 0.0545 mg/mL | EC50 = 0.0555 mg/mL |
Strain | MIC Value (mg/mL) | MBC Value (mg/mL) | ||||
---|---|---|---|---|---|---|
MAEopt | MAC | UAEopt | MAEopt | MAC | UAEopt | |
Escherichia coli ATCC 11775 | 25.00 | 25.00 | 25.00 | 25.00 | 50.00 | 25.00 |
Klebsiella pneumoniae ATCC 31488 | 25.00 | 25.00 | 12.50 | 25.00 | 25.00 | 25.00 |
Proteus mirabilis ATCC 12453 | 12.50 | 25.00 | 25.00 | 25.00 | 50.00 | 25.00 |
Pseudomonas aeruginosa ATCC 9027 | 25.00 | 25.00 | 25.00 | 25.00 | 50.00 | 50.00 |
Staphylococcus aureus ATCC 25923 | 12.50 | 12.50 | 12.50 | 25.00 | 25.00 | 25.00 |
Staphylococcus epidermidis JR-07 | 6.25 | 12.50 | 12.50 | 25.00 | 50.00 | 25.00 |
Micrococcus luteus JR-10 | 12.50 | 12.50 | 12.50 | 50.00 | 50.00 | 50.00 |
Bacillus cereus ATCC 11778 | 3.13 | 6.25 | 3.13 | 6.25 | 6.25 | 6.25 |
Bacillus subtilis PY79 | 12.50 | 12.50 | 12.50 | >50.00 | >50.00 | >50.00 |
Candida albicans ATCC 10231 | 12.50 | 6.25 | 12.50 | 25.00 | 25.00 | 25.00 |
Saccharomyces cerevisiae ATCC 9763 | ≤0.05 | 0.20 | ≤0.05 | ≤0.05 | 1.56 | ≤0.05 |
Extraction Method | Independent Variable | Factor Levels | ||
---|---|---|---|---|
−1 | 0 | 1 | ||
Temperature (°C) | 40 | 60 | 80 | |
UAE | Extraction time (min) | 40 | 60 | 80 |
Ultrasonic power (W/L) | 24 | 42 | 60 | |
Extraction time (min) | 15 | 25 | 35 | |
MAE | Ethanol concentration (%) | 30 | 50 | 70 |
Microwave power (W) | 400 | 600 | 800 |
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Gavarić, A.; Vladić, J.; Vujetić, J.; Radnović, D.; Volarić, A.; Živković, J.; Šavikin, K.; Vidović, S. The Application of Ultrasonic Waves and Microwaves to Improve Antihyperglycaemic and Antimicrobial Activities of Marrubium vulgare Extracts. Antibiotics 2022, 11, 1475. https://doi.org/10.3390/antibiotics11111475
Gavarić A, Vladić J, Vujetić J, Radnović D, Volarić A, Živković J, Šavikin K, Vidović S. The Application of Ultrasonic Waves and Microwaves to Improve Antihyperglycaemic and Antimicrobial Activities of Marrubium vulgare Extracts. Antibiotics. 2022; 11(11):1475. https://doi.org/10.3390/antibiotics11111475
Chicago/Turabian StyleGavarić, Aleksandra, Jelena Vladić, Jelena Vujetić, Dragan Radnović, Ana Volarić, Jelena Živković, Katarina Šavikin, and Senka Vidović. 2022. "The Application of Ultrasonic Waves and Microwaves to Improve Antihyperglycaemic and Antimicrobial Activities of Marrubium vulgare Extracts" Antibiotics 11, no. 11: 1475. https://doi.org/10.3390/antibiotics11111475