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. 2018 Oct 11;23(10):2598. doi: 10.3390/molecules23102598

Potential of Grape Wastes as a Natural Source of Bioactive Compounds

Guo-Yi Tang 1,†, Cai-Ning Zhao 1,†, Qing Liu 1, Xiao-Ling Feng 2, Xiao-Yu Xu 1, Shi-Yu Cao 1, Xiao Meng 1, Sha Li 3,*, Ren-You Gan 4, Hua-Bin Li 1,5,*
Editors: Luisella Verotta, Alessandra Napolitano
PMCID: PMC6222388  PMID: 30314259

Abstract

Grapes are widely used in the wine and juice industries, which can lead to massive amounts of waste, mostly grape peels and seeds. The antioxidant capacities, total phenolic and flavonoid contents and phenolic profiles of peels and seeds from 30 grape varieties were systemically assessed. The antioxidant activities of fat-soluble, water-soluble and insoluble-bound fractions of grape peels and seeds were evaluated using ferric-reducing antioxidant power and Trolox equivalent antioxidant capacity assays, and their total phenolic contents and total flavonoid contents were determined by the Folin-Ciocalteu method and AlCl3 colorimetry, respectively. It was found that the antioxidant capacities were diverse among different grape peels and seeds. Moreover, several phenolic compounds were identified and quantified, including gallic acid, cyanidin-3-glucoside, epicatechin, catechin gallate, ferulaic acid, rutin and resveratrol, which could contribute to the antioxidant capacities of these grape peels and seeds. Several grape wastes with strong antioxidant activity could be abundant sources of natural bioactive compounds, and have the potential for development into functional foods, food additives and pharmaceuticals.

Keywords: grape, peel, seed, waste, antioxidant capacity, bioactive compounds, phenol, flavonoid

1. Introduction

Grape is a famous fruit all over the world, and is widely used in wine and juice industries, which can lead to massive amounts of wastes, including grape peels and seeds [1]. It is reported that these wastes contain a variety of phytochemicals, especially phenols and flavonoids like anthocyanins, resveratrol, tannin and quercetin [2,3,4,5,6,7,8]. These bioactive components possess various outstanding bioactivities, such as antibacterial, anticancer, antioxidant, anti-inflammation and hepatic and cardiovascular protection effects [9,10,11,12,13], and have great safety and effectiveness advantages in preventing chronic diseases [14,15,16,17]. They can be used as raw materials to produce functional foods, food additives and pharmaceuticals [18,19,20,21,22,23]. Many factors can influence the composition and contents of bioactive compounds in fruits, like genotype, growth environment (soil, water, sunlight, etc.) and maturity, among which genotype usually has the greatest impact [24,25,26]. Thus, we could hypothesize that grapes with diverse genotypes should have different composition and contents of bioactive compounds, so it is worthwhile to assess the antioxidant capacities while determining the phenolic and flavonoid contents of peels and seeds from different grape varieties. In the present study, the antioxidant capacities of peels and seeds from 30 grape varieties were measured, and their total phenolic contents and total flavonoid contents were evaluated. In addition, the phenolic and flavonoid constituents were identified and quantified using HPLC analysis. This should prove helpful for the full utilization of grape peels and seeds.

2. Results and Discussion

2.1. Ferric Reducing Antioxidant Power (FRAP) of the Grape Peels and Seeds

The FRAP was used as one of the indices to assess antioxidant capacities of these grape peels and seeds. The FRAP assay is established on the basis of the ability that antioxidants reduce ferric ions to ferrous ions [27], which is a simple and commonly employed method to evaluate antioxidant capacity [28,29,30]. The FRAP values of these grape peels and seeds are presented in Table 1.

Table 1.

FRAP values of peels and seeds from 30 grape varieties.

Name of Grapes Place of Production Part of Grapes FARAP Values (μmol Fe(II)/g FW)
Fat-Soluble Fraction Water-Soluble Fraction Insoluble-Bound Fraction Total
Black Grape Yunnan, China Peel 99.407 ± 4.048 54.026 ± 1.833 0.273 ± 0.024 153.706 ± 5.904
Blackcurrant Grape California, CA, USA Peel 161.671 ± 5.628 91.100 ± 3.554 0.211 ± 0.003 252.983 ± 9.185
Flame Grape Xinjiang, China Peel 24.241 ± 2.288 40.931 ± 1.694 0.286 ± 0.022 65.457 ± 4.004
ragrant Green Grape Yunnan, China Peel 6.734 ± 0.364 11.407 ± 0.311 0.163 ± 0.005 18.304 ± 0.680
Golden Finger Grape California, CA, USA Peel 106.886 ± 5.354 115.195 ± 0.595 0.074 ± 0.005 222.155 ± 5.954
Green Grape Victoria, Australia Peel 20.336 ± 0.398 22.645 ± 1.450 0.245 ± 0.010 43.226 ± 1.858
Ito Kyoho Grape Yunnan, China Peel 63.526 ± 4.318 40.336 ± 1.193 0.170 ± 0.015 104.032 ± 5.526
Kyoho Grape Guangxi, China Peel 94.002 ± 2.110 26.026 ± 2.239 0.614 ± 0.032 120.642 ± 4.380
Kyoho Grape Liaoning, China Peel 59.621 ± 1.689 15.907 ± 0.655 0.164 ± 0.007 75.693 ± 2.351
Kyoho Grape Xinjiang, China Peel 90.217 ± 5.724 12.407 ± 1.111 0.092 ± 0.005 102.716 ± 6.840
Kyoho Grape Yunnan, China Peel 75.812 ± 5.004 24.264 ± 2.020 0.254 ± 0.023 100.331 ± 7.047
Pearl Black Grape Xinjiang, China Peel 84.479 ± 2.465 53.600 ± 3.536 0.144 ± 0.004 138.223 ± 6.005
Pearl Green Grape Xinjiang, China Peel 7.288 ± 0.648 20.907 ± 0.842 0.154 ± 0.013 28.350 ± 1.503
Pearl Green Grape Victoria, Australia Peel 36.955 ± 1.041 40.883 ± 1.636 0.211 ± 0.013 78.050 ± 2.689
Red Grape California, CA, USA Peel 42.169 ± 3.351 27.741 ± 0.975 0.083 ± 0.003 69.992 ± 4.329
Red Grape Guangxi, China Peel 35.645 ± 1.221 24.764 ± 0.446 0.131 ± 0.011 60.541 ± 1.678
Red Grape Xinjiang, China Peel 43.812 ± 1.782 21.693 ± 1.823 0.133 ± 0.013 65.638 ± 3.617
Red Grape Yunnan, China Peel 62.336 ± 2.133 35.431 ± 2.093 0.203 ± 0.005 97.969 ± 4.231
Rose Black Grape Xinjiang, China Peel 62.526 ± 3.635 65.717 ± 5.437 0.387 ± 0.030 128.630 ± 9.103
Rose Black Grape Yunnan, China Peel 59.383 ± 2.580 39.741 ± 1.034 0.408 ± 0.033 99.532 ± 3.646
Seedless Black Grape California, CA, USA Peel 106.674 ± 2.619 90.669 ± 8.983 0.401 ± 0.036 197.742 ± 11.638
Seedless Black Grape Xinjiang, China Peel 66.526 ± 2.269 67.074 ± 3.610 0.219 ± 0.003 133.819 ± 5.882
Seedless Dew Grape Xinjiang, China Peel 18.241 ± 1.656 31.136 ± 1.262 0.295 ± 0.015 49.672 ± 2.933
Seedless Green Grape Xinjiang, China Peel 7.264 ± 0.707 25.169 ± 1.567 0.131 ± 0.010 32.564 ± 2.284
Seedless Red Grape California, CA, USA Peel 53.657 ± 0.051 71.217 ± 4.113 0.094 ± 0.003 124.967 ± 4.166
Seedless Red Grape Victoria, Australia Peel 65.669 ± 2.402 65.288 ± 5.794 0.294 ± 0.003 131.251 ± 8.198
Seedless Red Grape Xinjiang, China Peel 24.026 ± 0.664 26.002 ± 1.329 0.138 ± 0.005 50.167 ± 1.998
Seedless Red Grape Yunnan, China Peel 25.669 ± 0.972 31.979 ± 1.608 0.217 ± 0.005 57.864 ± 2.586
Summer Black Grape Shaanxi, China Peel 85.121 ± 6.061 72.407 ± 4.772 0.233 ± 0.013 157.761 ± 10.846
Summer Black Grape Xinjiang, China Peel 56.883 ± 5.017 46.312 ± 3.526 0.379 ± 0.012 103.574 ± 8.555
Black Grape Yunnan, China Seed 692.019 ± 18.217 144.767 ± 3.348 0.456 ± 0.013 837.242 ± 21.578
Ito Kyoho Grape Yunnan, China Seed 301.924 ± 4.439 64.148 ± 4.014 0.424 ± 0.000 366.495 ± 8.452
Kyoho Grape Xinjiang, China Seed 371.448 ± 13.718 50.243 ± 3.295 0.436 ± 0.023 422.127 ± 17.036
Kyoho Grape Guangxi, China Seed 250.876 ± 8.208 59.671 ± 3.369 1.881 ± 0.184 312.429 ± 11.760
Kyoho Grape Yunnan, China Seed 283.638 ± 22.325 44.148 ± 3.996 0.868 ± 0.052 328.654 ± 26.373
Pearl Black Grape Xinjiang, China Seed 726.495 ± 23.487 131.243 ± 11.987 0.383 ± 0.033 858.121 ± 35.507
Red Grape Yunnan, China Seed 502.876 ± 27.668 112.862 ± 1.918 0.747 ± 0.043 616.485 ± 29.629
Red Grape Guangxi, China Seed 351.067 ± 19.144 122.576 ± 3.677 0.528 ± 0.005 474.170 ± 22.825
Red Grape Xinjiang, China Seed 450.305 ± 15.144 111.243 ± 4.267 0.470 ± 0.027 562.018 ± 19.437
Red Grape California, CA, USA Seed 401.924 ± 16.337 117.148 ± 3.570 1.319 ± 0.068 520.390 ± 19.974
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For the 30 grape peels, the total FRAP values varied from 18.304 ± 0.680 to 252.983 ± 9.185 μmol Fe(II)/g fresh weight (FW) with a 14-fold difference. Blackcurrant Grape (California, CA, USA), Golden Finger Grape (California, CA, USA), Seedless Black Grape (California, CA, USA), Summer Black Grape (Shaanxi, China) and Black Grape (Yunnan, China) possessed the top-five antioxidant capacities, which were 252.983 ± 9.185, 222.155 ± 5.954, 197.742 ± 11.638, 157.761 ± 10.846 and 153.706 ± 5.904 μmol Fe(II)/g FW, respectively. Fragrant Green Grape (Yunnan, China) possessed the lowest antioxidant capacity, which was 18.304 ± 0.680 μmol Fe(II)/g FW. In addition, the ranges of FRAP values for three fractions were in a decreasing order: fat-soluble (6.734 ± 0.364 to 161.671 ± 5.628 μmol Fe(II)/g FW) > water-soluble (11.407 ± 0.311 to 115.195 ± 0.595 μmol Fe(II)/g FW) > insoluble-bound (0.074 ± 0.005 to 0.614 ± 0.032 μmol Fe(II)/g FW) (p = 0.030, p < 0.001, respectively).

For the 10 grape seeds, the total FRAP values varied from 312.429 ± 11.760 to 858.121 ± 35.507 μmol Fe(II)/g FW with a 3-fold difference. Pearl Black Grape (Xinjiang, China), Black Grape (Yunnan, China), Red Grape (Yunnan, China), Red Grape (Xinjiang, China) and Red Grape (California, CA, USA) possessed the top-five antioxidant capacities, which were 858.121 ± 35.507, 837.242 ± 21.578, 616.485 ± 29.629, 562.018 ± 19.437 and 520.390 ± 19.974, respectively. Kyoho Grape (Guangxi, China) possessed the lowest antioxidant capacity, which was 312.429 ± 11.760 μmol Fe(II)/g FW. In addition, the ranges of FRAP values for three fractions were in a decreasing order: fat-soluble (250.876 ± 8.208 to 726.495 ± 23.487 μmol Fe(II)/g FW) > water-soluble (44.148 ± 3.996 to 144.767 ± 3.348 μmol Fe(II)/g FW) > insoluble-bound (0.383 ± 0.033 to 1.881 ± 0.184 μmol Fe(II)/g FW) (p < 0.001, p = 0.038, respectively).

According to the results described above, the FRAP values of fat-soluble fractions were generally higher than those of water-soluble fractions, which were distinctly higher than those of insoluble-bound fractions. These results indicated that the antioxidants responsible for the reducing power of grape peels and seeds were most fat-soluble compounds with some water-soluble and a little insoluble-bound ones. When evaluating total antioxidant capacities of grape peels and seeds, all of the three fractions should be taken into consideration. In addition, the FRAP values of grape seeds were apparently higher than those of grape peels (p < 0.001). As compared to other materials, the FRAP values of the tested grape peels were higher than those of most edible macro-fungi, vegetables, fruits and fruit wastes (peels and seeds) [31,32,33,34], and also higher than those of some wild fruits and edible and wild flowers [35,36]. Moreover, the FRAP values of the tested grape seeds were higher than those of most edible macro-fungi, vegetables, wild fruits, edible and wild flowers, fruits and fruit wastes (peels and seeds) [31,32,33,34,35,36], and higher than those of some medicinal plants [37]. So grape peels and seeds could be abundant resources of natural antioxidants with great potential to produce functional foods, food additives and pharmaceuticals.

2.2. Trolox Equivalent Antioxidant Capacity (TEAC) of the Grape Peels and Seeds

Most natural antioxidants are multifunctional, and the antioxidant capacities of plant samples are generally impacted by multiple factors, such as the extraction solvent, extraction method and measurement method, leading to difficulty to completely demonstrate antioxidant capacities using a single method. Therefore, an authentic antioxidant assessing system requires evaluations of multiple aspects, and it is essential to conduct different experiments to assess the antioxidant activity which might be associated with diverse mechanisms of action [38]. The TEAC assay is a simple, fast, repeatable and widely used method for the evaluation of antioxidant capacity [39,40]. The TEAC assay is on the basis of the capability of antioxidants to scavenge the ABTS•+ radical, and can be used for measuring antioxidant capacities of fat-soluble, water-soluble and insoluble-bound components in the same sample [41]. As reported, vitamin C, vitamin E, butylated hydroxytoluene, butylated hydroxyanisole and Trolox were often applied as reference standards [42,43]. Here, Trolox was employed. The TEAC values of the peels and seeds from 30 grape varieties are displayed in Table 2.

Table 2.

TEAC values of peels and seeds from 30 grape varieties.

Name of Grapes Place of Production Part of Grapes TEAC Values (μmol Trolox/g FW)
Fat-Soluble Fraction Water-Soluble Fraction Insoluble-Bound Fraction Total
Black Grape Yunnan, China Peel 58.264 ± 2.194 23.4742 ± 0.637 0.315 ± 0.030 82.053 ± 2.861
Blackcurrant Grape California, CA, USA Peel 84.463 ± 1.361 39.1097 ± 1.59 0.167 ± 0.015 123.740 ± 2.969
Flame Grape Xinjiang, China Peel 14.572 ± 1.001 9.0073 ± 0.140 0.209 ± 0.016 23.788 ± 1.157
Fragrant Green Grape Yunnan, China Peel 2.293 ± 0.133 2.7259 ± 0.061 0.156 ± 0.015 5.1760 ± 0.209
Golden Finger Grape California, CA, USA Peel 68.596 ± 5.519 29.4711 ± 0.381 0.039 ± 0.003 98.106 ± 5.902
Green Grape Victoria, Australia Peel 13.165 ± 0.524 7.4739 ± 0.314 0.166 ± 0.016 20.804 ± 0.854
Ito Kyoho Grape Yunnan, China Peel 34.777 ± 2.078 16.1091 ± 0.714 0.242 ± 0.023 51.128 ± 2.815
Kyoho Grape Guangxi, China Peel 31.151 ± 1.088 3.8408 ± 0.206 0.138 ± 0.003 35.130 ± 1.297
Kyoho Grape Liaoning, China Peel 42.555 ± 0.447 5.3211 ± 0.081 0.069 ± 0.003 47.945 ± 0.531
Kyoho Grape Xinjiang, China Peel 50.852 ± 3.082 12.8820 ± 0.979 0.383 ± 0.029 64.117 ± 4.090
Kyoho Grape Yunnan, China Peel 38.092 ± 1.912 12.0422 ± 1.146 0.163 ± 0.008 50.297 ± 3.065
Pearl Black Grape Xinjiang, China Peel 48.202 ± 0.567 30.2866 ± 2.763 0.075 ± 0.005 78.563 ± 3.336
Pearl Green Grape Xinjiang, China Peel 3.267 ± 0.254 6.0273 ± 0.026 0.141 ± 0.013 9.435 ± 0.293
Pearl Green Grape Victoria, Australia Peel 21.066 ± 0.750 20.9262 ± 0.525 0.105 ± 0.010 42.097 ± 1.285
Red Grape California, CA, USA Peel 34.654 ± 0.605 15.7459 ± 0.266 0.158 ± 0.010 50.557 ± 0.881
Red Grape Guangxi, China Peel 21.460 ± 0.485 6.5821 ± 0.043 0.098 ± 0.008 28.141 ± 0.536
Red Grape Xinjiang, China Peel 26.268 ± 2.316 9.8911 ± 0.620 0.134 ± 0.011 36.293 ± 2.947
Red Grape Yunnan, China Peel 24.813 ± 1.079 15.1921 ± 0.525 0.028 ± 0.002 40.033 ± 1.606
Rose Black Grape Xinjiang, China Peel 35.038 ± 1.647 29.0777 ± 2.282 0.237 ± 0.016 64.353 ± 3.944
Rose Black Grape Yunnan, China Peel 30.936 ± 1.431 19.7177 ± 0.469 0.216 ± 0.009 50.869 ± 1.909
Seedless Black Grape California, CA, USA Peel 34.388 ± 0.258 27.5440 ± 1.616 0.116 ± 0.008 62.047 ± 1.882
Seedless Black Grape Xinjiang, China Peel 62.835 ± 0.877 38.0697 ± 2.950 0.246 ± 0.012 101.151 ± 3.839
Seedless Dew Grape Xinjiang, China Peel 11.461 ± 0.428 7.9079 ± 0.043 0.252 ± 0.003 19.621 ± 0.473
Seedless Green Grape Xinjiang, China Peel 4.579 ± 0.363 10.3781 ± 0.402 0.083 ± 0.008 15.040 ± 0.773
Seedless Red Grape California, CA, USA Peel 16.143 ± 0.473 13.5667 ± 0.159 0.150 ± 0.010 29.860 ± 0.642
Seedless Red Grape Victoria, Australia Peel 14.900 ± 0.758 11.7903 ± 0.731 0.033 ± 0.003 26.724 ± 1.491
Seedless Red Grape Xinjiang, China Peel 29.336 ± 1.267 28.2014 ± 1.974 0.044 ± 0.003 57.582 ± 3.243
Seedless Red Grape Yunnan, China Peel 36.584 ± 1.474 21.6865 ± 1.676 0.103 ± 0.005 58.374 ± 3.155
Summer Black Grape Shaanxi, China Peel 51.789 ± 1.878 30.2866 ± 2.195 0.167 ± 0.013 82.242 ± 4.086
Summer Black Grape Xinjiang, China Peel 31.496 ± 2.283 28.6149 ± 1.900 0.246 ± 0.009 60.358 ± 4.192
Black Grape Yunnan, China Seed 329.773 ± 5.710 62.5184 ± 0.510 0.287 ± 0.015 392.577 ± 6.236
Ito Kyoho Grape Yunnan, China Seed 181.739 ± 1.029 31.7674 ± 1.296 0.295 ± 0.023 213.802 ± 2.348
Kyoho Grape Xinjiang, China Seed 231.921 ± 9.528 24.5545 ± 1.907 0.207 ± 0.005 256.682 ± 11.440
Kyoho Grape Guangxi, China Seed 192.411 ± 9.735 38.4204 ± 1.567 1.320 ± 0.071 232.152 ± 11.373
Kyoho Grape Yunnan, China Seed 176.024 ± 8.804 31.2584 ± 1.739 0.532 ± 0.031 207.815 ± 10.573
Pearl Black Grape Xinjiang, China Seed 409.190 ± 19.195 64.1050 ± 0.106 0.159 ± 0.003 473.454 ± 19.303
Red Grape Yunnan, China Seed 274.455 ± 11.707 55.1126 ± 1.364 0.587 ± 0.015 330.155 ± 13.086
Red Grape Guangxi, China Seed 199.613 ± 6.407 54.3559 ± 1.308 0.380 ± 0.005 254.349 ± 7.720
Red Grape Xinjiang, China Seed 246.250 ± 7.908 47.3937 ± 0.889 0.266 ± 0.007 293.910 ± 8.804
Red Grape California, CA, USA Seed 229.045 ± 7.867 62.7832 ± 0.696 0.520 ± 0.048 292.349 ± 8.610
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For the 30 grape peels, the total TEAC values ranged from 5.176 ± 0.209 to 123.740 ± 2.969 μmol Trolox/g FW with a 24-fold difference. Blackcurrant Grape (California, CA, USA), Seedless Black Grape (Xinjiang, China), Golden Finger Grape (California, CA, USA), Summer Black Grape (Shaanxi, China) and Black Grape (Yunnan, China) possessed the top-five free radical scavenging capacities, which were 123.740 ± 2.969, 101.151 ± 3.839, 98.106 ± 5.902, 82.242 ± 4.086 and 82.053 ± 2.861 μmol Trolox/g FW, respectively. Fragrant Green Grape (Yunnan, China) possessed the lowest free radical scavenging capacity, which was 5.176 ± 0.209 μmol Trolox/g FW. In addition, the ranges of TEAC values for three fractions were in a decreasing order: fat-soluble (2.293 ± 0.133 to 84.463 ± 1.361 μmol trolox/g FW) > water-soluble (2.726 ± 0.061 to 39.110 ± 1.592 μmol Trolox/g FW) > insoluble-bound (0.028 ± 0.002 to 0.383 ± 0.029 μmol trolox/g FW) (p < 0.001, p < 0.001, respectively).

For the 10 grape seeds, the total TEAC values ranged from 207.815 ± 10.573 to 473.454 ± 19.303 μmol Trolox/g FW with a 2-fold difference. Pearl Black Grape (Xinjiang, China), Black Grape (Yunnan, China), Red Grape (Yunnan, China), Red Grape (Xinjiang, China) and Red Grape (California, CA, USA) possessed the top-five free radical scavenging capacities, which were 473.454 ± 19.303, 392.577 ± 6.236, 330.155 ± 13.086, 293.910 ± 8.804 and 292.349 ± 8.610 μmol Trolox/g FW, respectively. Kyoho Grape (Yunnan, China) possessed the lowest free radical scavenging capacity, which was 207.815 ± 10.573 μmol Trolox/g FW. In addition, the ranges of TEAC values for three fractions were in a decreasing order: fat-soluble (181.739 ± 1.029 to 409.190 ± 19.195 μmol trolox/g FW) > water-soluble (24.555 ± 1.907 to 64.105 ± 0.106 μmol trolox/g FW) > insoluble-bound (0.159 ± 0.003 to 1.320 ± 0.071 μmol trolox/g FW) (p < 0.001, p = 0.023, respectively).

As seen from the description before, the TEAC values of fat-soluble fractions were generally higher than those of water-soluble fractions, which were distinctly higher than those of insoluble-bound fractions. It meant that the antioxidants, which were responsible for the free radical scavenging activities of grape peels and seeds, were most fat-soluble compounds with some water soluble and a little insoluble-bound ones. When the total antioxidant capacities of grape peels and seeds are about to be assessed, three fractions should all be counted in. In addition, the TEAC values of the grape seeds were extremely higher than those of the grape peels (p < 0.001). Besides, the TEAC values of the grape peels were higher than those of most edible macro-fungi, vegetables, fruits and fruit waste (peels and seeds) [31,32,33,34], and higher than those of some wild fruits and edible and wild flowers [35,36]. Furthermore, the TEAC values of the grape seeds were higher than those of most edible macro-fungi, vegetables, edible and wild flowers, fruits and fruit waste (peels and seeds) [31,32,33,34,35,36], and higher than those of some wild fruits and medicinal plants [37], so grape peels and seeds could be developed into functional foods, food additives and pharmaceuticals regarding antioxidants.

2.3. Total Phenolic Contents (TPC) of 30 Grape Peels and 10 Grape Seeds

The TPC values of these grape peels and seeds were determined by the Folin-Ciocalteu method, which is based on the reaction that electrons are transferred from phenolic compounds to the Folin-Ciocalteu reagent in alkaline medium, and is a simple, rapid and reproducible method [44]. The TPC values of these grape peels and seeds are given in Table 3.

Table 3.

TPC values of peels and seeds from 30 grape varieties.

Name of Grapes Place of Production Part of Grapes TPC Values (mg GAE/g FW)
Fat-Soluble Fraction Water-Soluble Fraction Insoluble-Bound Fraction Total
Black Grape Yunnan, China Peel 8.992 ± 0.646 5.516 ± 0.091 0.066 ± 0.006 14.574 ± 0.742
Blackcurrant Grape California, CA, USA Peel 16.529 ± 0.463 9.171 ± 0.430 0.025 ± 0.001 25.724 ± 0.894
Flame Grape Xinjiang, China Peel 2.5485 ± 0.173 3.782 ± 0.144 0.029 ± 0.002 6.356 ± 0.319
Fragrant Green Grape Yunnan, China Peel 0.811 ± 0.025 0.754 ± 0.037 0.024 ± 0.001 1.588 ± 0.062
Golden Finger Grape California, CA, USA Peel 6.443 ± 0.488 6.673 ± 0.024 0.015 ± 0.001 13.131 ± 0.514
Green Grape Victoria, Australia Peel 2.530 ± 0.028 2.366 ± 0.087 0.029 ± 0.002 4.925 ± 0.118
Ito Kyoho Grape Yunnan, China Peel 6.778 ± 0.300 3.774 ± 0.139 0.047 ± 0.004 10.599 ± 0.444
Kyoho Grape Guangxi, China Peel 6.809 ± 0.176 1.177 ± 0.061 0.018 ± 0.001 8.003 ± 0.239
Kyoho Grape Liaoning, China Peel 8.719 ± 0.341 6.752 ± 0.664 0.012 ± 0.001 15.483 ± 1.006
Kyoho Grape Xinjiang, China Peel 9.341 ± 0.517 2.935 ± 0.095 0.072 ± 0.002 12.348 ± 0.614
Kyoho Grape Yunnan, China Peel 7.689 ± 0.713 2.962 ± 0.151 0.036 ± 0.003 10.687 ± 0.866
Pearl Black Grape Xinjiang, China Peel 8.374 ± 0.210 6.944 ± 0.686 0.020 ± 0.001 15.338 ± 0.897
Pearl Green Grape Xinjiang, China Peel 1.138 ± 0.014 1.872 ± 0.083 0.027 ± 0.002 3.037 ± 0.099
Pearl Green Grape Victoria, Australia Peel 4.189 ± 0.089 4.618 ± 0.148 0.027 ± 0.002 8.833 ± 0.239
Red Grape California, CA, USA Peel 6.624 ± 0.233 3.528 ± 0.178 0.037 ± 0.001 10.189 ± 0.412
Red Grape Guangxi, China Peel 4.006 ± 0.400 2.331 ± 0.175 0.022 ± 0.001 6.359 ± 0.575
Red Grape Xinjiang, China Peel 4.935 ± 0.242 2.398 ± 0.043 0.029 ± 0.001 7.362 ± 0.286
Red Grape Yunnan, China Peel 4.683 ± 0.325 3.532 ± 0.084 0.011 ± 0.001 8.226 ± 0.410
Rose Black Grape Xinjiang, China Peel 6.524 ± 0.295 6.171 ± 0.486 0.043 ± 0.004 12.738 ± 0.786
Rose Black Grape Yunnan, China Peel 6.319 ± 0.560 4.669 ± 0.086 0.045 ± 0.002 11.032 ± 0.648
Seedless Black Grape California, CA, USA Peel 6.758 ± 0.193 6.512 ± 0.345 0.023 ± 0.000 13.293 ± 0.538
Seedless Black Grape Xinjiang, China Peel 11.426 ± 0.278 8.679 ± 0.703 0.048 ± 0.002 20.153 ± 0.983
Seedless Dew Grape Xinjiang, China Peel 2.372 ± 0.146 2.626 ± 0.185 0.041 ± 0.001 5.039 ± 0.332
Seedless Green Grape Xinjiang, China Peel 2.795 ± 0.026 2.774 ± 0.099 0.025 ± 0.002 5.594 ± 0.126
Seedless Red Grape California, CA, USA Peel 2.992 ± 0.052 2.933 ± 0.041 0.028 ± 0.002 5.953 ± 0.095
Seedless Red Grape Victoria, Australia Peel 2.839 ± 0.144 2.764 ± 0.113 0.016 ± 0.000 5.619 ± 0.257
Seedless Red Grape Xinjiang, China Peel 5.667 ± 0.086 6.553 ± 0.308 0.012 ± 0.001 12.232 ± 0.395
Seedless Red Grape Yunnan, China Peel 6.599 ± 0.110 6.547 ± 0.611 0.023 ± 0.002 13.169 ± 0.723
Summer Black Grape Shaanxi, China Peel 8.624 ± 0.535 6.169 ± 0.342 0.029 ± 0.002 14.822 ± 0.879
Summer Black Grape Xinjiang, China Peel 5.606 ± 0.078 5.036 ± 0.318 0.043 ± 0.001 10.685 ± 0.397
Black Grape Yunnan, China Seed 57.169 ± 0.954 13.150 ± 0.249 0.057 ± 0.004 70.376 ± 1.207
Ito Kyoho Grape Yunnan, China Seed 29.966 ± 0.098 7.300 ± 0.403 0.045 ± 0.002 37.311 ± 0.503
Kyoho Grape Xinjiang, China Seed 37.527 ± 0.483 5.593 ± 0.365 0.054 ± 0.005 43.174 ± 0.853
Kyoho Grape Guangxi, China Seed 29.998 ± 1.621 7.073 ± 0.139 0.214 ± 0.009 37.285 ± 1.769
Kyoho Grape Yunnan, China Seed 28.584 ± 2.017 5.947 ± 0.411 0.098 ± 0.006 34.628 ± 2.435
Pearl Black Grape Xinjiang, China Seed 58.372 ± 0.692 12.833 ± 0.069 0.039 ± 0.001 71.244 ± 0.762
Red Grape Yunnan, China Seed 44.714 ± 1.636 10.967 ± 0.269 0.090 ± 0.008 55.771 ± 1.912
Red Grape Guangxi, China Seed 33.917 ± 1.436 11.333 ± 0.279 0.062 ± 0.006 45.312 ± 1.722
Red Grape Xinjiang, China Seed 40.811 ± 1.199 10.451 ± 0.374 0.053 ± 0.005 51.315 ± 1.578
Red Grape California, CA, USA Seed 37.104 ± 1.315 11.971 ± 0.253 0.095 ± 0.002 49.170 ± 1.570
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For the 30 grape peels, the total TPC values varied from 1.588 ± 0.062 to 25.724 ± 0.894 mg GAE/g FW with a 16-fold difference. Blackcurrant Grape (California, CA, USA), Seedless Black Grape (Xinjiang, China), Kyoho Grape (Liaoning, China), Pearl Black Grape (Xinjiang, China) and Summer Black Grape (Shaanxi, China) had the top-five total phenolic contents, which were 25.724 ± 0.894, 20.153 ± 0.983, 15.483 ± 1.006, 15.338 ± 0.897 and 14.822 ± 0.879 mg GAE/g FW, respectively. Fragrant Green Grape (Yunnan, China) had the lowest total phenolic content, which was 1.588 ± 0.062 mg GAE/g FW. In addition, the ranges of TPC values for three fractions were in a decreasing order: fat-soluble (0.811 ± 0.025 to 16.528 ± 0.463 mg GAE/g FW) > water-soluble (0.754 ± 0.037 to 9.1705 ± 0.4299 mg GAE/g FW) > insoluble-bound (0.011 ± 0.001 to 0.072 ± 0.002 mg GAE/g FW) (p = 0.009, p < 0.001, respectively).

For the 10 grape seeds, the total TPC values varied from 34.628 ± 2.435 to 71.244 ± 0.762 mg GAE/g FW with a 2-fold difference. Pearl Black Grape (Xinjiang, China), Black Grape (Yunnan, China), Red Grape (Yunnan, China), Red Grape (Xinjiang, China) and Red Grape (California, CA, USA) had the top-five total phenolic contents, which were 71.244 ± 0.762, 70.376 ± 1.207, 55.771 ± 1.912, 51.315 ± 1.578 and 49.170 ± 1.570 mg GAE/g FW, respectively. Kyoho Grape (Yunnan, China) had the lowest total phenolic content, which was 34.628 ± 2.435 mg GAE/g FW. In addition, the ranges of TPC values for three fractions were in a decreasing order: fat-soluble (28.584 ± 2.017 to 58.372 ± 0.692 mg GAE/g FW) > water-soluble (5.593 ± 0.365 to 13.150 ± 0.249 mg GAE/g FW) > insoluble-bound (0.039 ± 0.001 to 0.214 ± 0.009 mg GAE/g FW) (p < 0.01, p = 0.02, respectively).

Based on the above demonstration, the TPC values of the grape seeds were drastically higher than those of the grape peels (p < 0.001). Besides, the TPC values of the grape peels were higher than those of most edible macro-fungi, vegetables, fruits and fruit waste (peels and seeds) [31,32,33,34], and higher than those of some wild fruits and edible and wild flowers [35,36]. Moreover, the TPC values of the grape seeds were higher than those of most edible macro-fungi, vegetables, edible and wild flowers, wild fruits, fruits and fruit wastes (peels and seeds) [31,32,33,34,35,36], and higher than those of some medicinal plants [37], so grape peels and seeds could be used to extract phenols with further applications in the functional food, pharmaceutical, food additive and cosmetic industries. Furthermore, it should be pointed out that some non-phenolic components such as organic acids and sugars, which also possess reducing capacity, could affect the measurement of total phenolic contents determined by the Folin–Ciocalteu method, leading to overestimated total phenolic contents [45,46]. In addition, varied phenols might response to the Folin–Ciocalteu reagent differently and several flavonoids present low responses, which might cause an underestimate of total phenolic contents [47,48,49].

2.4. Total Flavonoid Contents (TFC) of the Grape Peels and Seeds

The TFC values of these grape peels and seeds were estimated by the AlCl3 colorimetry method according to the literature reported by Kalia et al., which is based on the reaction that the 3-hydroxy-4-hydroxyl or 5-hydroxy-4-carbonyl or o-2-phenolic hydroxyl of flavonoids is combined with Al3+ to form a red complex under an alkaline condition, and is a simple, rapid and repeatable method [50]. The TFC values of these grape peels and seeds are given in Table 4.

Table 4.

TFC values of peels and seeds from 30 grape varieties.

Name of Grapes Place of Production Part of Grapes TFC Values (mg QE/g FW)
Fat-Soluble Fraction Water-Soluble Fraction Insoluble-Bound Fraction Total
Black Grape Yunnan, China Peel 0.688 ± 0.021 0.260 ± 0.009 0.014 ± 0.001 0.962 ± 0.031
Blackcurrant Grape California, CA, USA Peel 1.017 ± 0.087 0.381 ± 0.003 0.010 ± 0.000 1.408 ± 0.091
Flame Grape Xinjiang, China Peel 0.175 ± 0.011 0.139 ± 0.005 0.010 ± 0.000 0.324 ± 0.016
Fragrant Green Grape Yunnan, China Peel 0.320 ± 0.027 0.042 ± 0.001 0.081 ± 0.004 0.443 ± 0.032
Golden Finger Grape California, CA, USA Peel 0.760 ± 0.059 0.362 ± 0.025 0.008 ± 0.000 1.130 ± 0.084
Green Grape Victoria, Australia Peel 0.232 ± 0.011 0.075 ± 0.002 0.010 ± 0.001 0.318 ± 0.014
Ito Kyoho Grape Yunnan, China Peel 0.302 ± 0.025 0.090 ± 0.005 0.055 ± 0.002 0.448 ± 0.032
Kyoho Grape Guangxi, China Peel 0.425 ± 0.017 0.072 ± 0.002 0.013 ± 0.001 0.510 ± 0.020
Kyoho Grape Liaoning, China Peel 0.326 ± 0.022 0.049 ± 0.003 0.008 ± 0.000 0.384 ± 0.026
Kyoho Grape Xinjiang, China Peel 0.402 ± 0.023 0.071 ± 0.006 0.016 ± 0.001 0.488 ± 0.029
Kyoho Grape Yunnan, China Peel 0.229 ± 0.023 0.063 ± 0.005 0.012 ± 0.001 0.304 ± 0.029
Pearl Black Grape Xinjiang, China Peel 0.398 ± 0.020 0.133 ± 0.011 0.059 ± 0.001 0.590 ± 0.032
Pearl Green Grape Xinjiang, China Peel 0.109 ± 0.002 0.052 ± 0.002 0.015 ± 0.001 0.176 ± 0.005
Pearl Green Grape Victoria, Australia Peel 0.192 ± 0.002 0.074 ± 0.002 0.011 ± 0.000 0.276 ± 0.004
Red Grape California, CA, USA Peel 0.504 ± 0.023 0.115 ± 0.006 0.013 ± 0.001 0.633 ± 0.029
Red Grape Guangxi, China Peel 0.343 ± 0.019 0.104 ± 0.005 0.011 ± 0.000 0.458 ± 0.024
Red Grape Xinjiang, China Peel 0.283 ± 0.018 0.076 ± 0.004 0.009 ± 0.000 0.368 ± 0.022
Red Grape Yunnan, China Peel 0.238 ± 0.008 0.065 ± 0.005 0.010 ± 0.001 0.313 ± 0.013
Rose Black Grape Xinjiang, China Peel 0.425 ± 0.010 0.212 ± 0.017 0.012 ± 0.001 0.649 ± 0.027
Rose Black Grape Yunnan, China Peel 0.326 ± 0.015 0.132 ± 0.006 0.010 ± 0.001 0.468 ± 0.022
Seedless Black Grape California, CA, USA Peel 0.326 ± 0.028 0.197 ± 0.004 0.012 ± 0.001 0.535 ± 0.033
Seedless Black Grape Xinjiang, China Peel 0.642 ± 0.031 0.331 ± 0.026 0.009 ± 0.000 0.982 ± 0.056
Seedless Dew Grape Xinjiang, China Peel 0.163 ± 0.003 0.092 ± 0.003 0.012 ± 0.001 0.266 ± 0.007
Seedless Green Grape Xinjiang, China Peel 0.126 ± 0.009 0.061 ± 0.000 0.012 ± 0.001 0.198 ± 0.010
Seedless Red Grape California, CA, USA Peel 0.199 ± 0.005 0.075 ± 0.002 0.017 ± 0.000 0.291 ± 0.006
Seedless Red Grape Victoria, Australia Peel 0.226 ± 0.010 0.091 ± 0.003 0.008 ± 0.000 0.325 ± 0.013
Seedless Red Grape Xinjiang, China Peel 0.321 ± 0.013 0.106 ± 0.000 0.008 ± 0.001 0.435 ± 0.014
Seedless Red Grape Yunnan, China Peel 0.317 ± 0.001 0.125 ± 0.010 0.009 ± 0.000 0.451 ± 0.011
Summer Black Grape Shaanxi, China Peel 0.317 ± 0.015 0.111 ± 0.008 0.014 ± 0.001 0.441 ± 0.023
Summer Black Grape Xinjiang, China Peel 0.403 ± 0.010 0.196 ± 0.015 0.011 ± 0.001 0.609 ± 0.025
Black Grape Yunnan, China Seed 1.126 ± 0.044 0.173 ± 0.003 0.041 ± 0.001 1.339 ± 0.048
Ito Kyoho Grape Yunnan, China Seed 2.989 ± 0.017 0.109 ± 0.005 0.024 ± 0.000 3.122 ± 0.022
Kyoho Grape Xinjiang, China Seed 3.786 ± 0.182 0.078 ± 0.006 0.020 ± 0.001 3.884 ± 0.189
Kyoho Grape Guangxi, China Seed 2.636 ± 0.238 0.096 ± 0.004 0.033 ± 0.002 2.765 ± 0.245
Kyoho Grape Yunnan, China Seed 1.165 ± 0.051 0.074 ± 0.006 0.023 ± 0.002 1.262 ± 0.059
Pearl Black Grape Xinjiang, China Seed 3.378 ± 0.167 0.101 ± 0.002 0.146 ± 0.006 3.626 ± 0.176
Red Grape Yunnan, China Seed 3.792 ± 0.211 0.126 ± 0.001 0.038 ± 0.001 3.957 ± 0.213
Red Grape Guangxi, China Seed 1.165 ± 0.022 0.157 ± 0.010 0.040 ± 0.002 1.361 ± 0.033
Red Grape Xinjiang, China Seed 2.536 ± 0.227 0.114 ± 0.000 0.030 ± 0.001 2.680 ± 0.227
Red Grape California, CA, USA Seed 1.024 ± 0.044 0.086 ± 0.008 0.020 ± 0.002 1.130 ± 0.054
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For the 30 grape peels, the total TFC values ranged from 0.176 ± 0.005 to 1.408 ± 0.091 mg QE/g FW with an 8-fold difference. Blackcurrant Grape (California, CA, USA), Golden Finger Grape (California, CA, USA), Seedless Black Grape (Xinjiang, China), Black Grape (Yunnan, China) and Rose Black Grape (Xinjiang, China) had the top-five total flavonoid contents, which were 1.408 ± 0.091, 1.130 ± 0.084, 0.982 ± 0.056, 0.962 ± 0.031 and 0.649 ± 0.027 mg QE/g FW, respectively. Pearl Green Grape (Xinjiang, China) had the lowest total flavonoid content, which was 0.176 ± 0.005 mg QE/g FW. In addition, the ranges of TPC values for three fractions were in a decreasing order: fat-soluble (0.109 ± 0.002 to 1.017 ± 0.087 mg QE/g FW) > water-soluble (0.042 ± 0.001 to 0.381 ± 0.003 mg QE/g FW) > insoluble-bound (0.008 ± 0.000 mg QE/g FW to 0.081 ± 0.004 mg QE/g FW) (p < 0.001, p = 0.001, respectively).

For the 10 grape seeds, the total TFC values ranged from 1.130 ± 0.054 mg QE/g FW to 3.957 ± 0.213 mg QE/g FW with a 4-fold difference. Red Grape (Yunnan, China), Kyoho Grape (Xinjiang, China), Pearl Black Grape (Xinjiang, China), Ito Kyoho Grape(Yunnan, China) and Kyoho Grape (Guangxi, China) had the top-five total flavonoid contents, which were 3.957 ± 0.213, 3.884 ± 0.189, 3.626 ± 0.176, 3.122 ± 0.022 and 2.765 ± 0.245 mg QE/g FW, respectively. Red Grape (California, CA, USA) had the lowest total flavonoid content, which was 1.130 ± 0.054 mg QE/g FW. In addition, the ranges of TPC values for three fractions were in a decreasing order: fat-soluble (1.024 ± 0.044 to 3.792 ± 0.211 mg QE/g FW) > water-soluble (0.074 ± 0.006 mg QE/g FW to 0.173 ± 0.003 mg QE/g FW) > insoluble-bound (0.020 ± 0.001 to 0.146 ± 0.006 mg QE/g FW) (p < 0.001, p = 0.815, respectively).

As illustrated before, the TFC values of the grape seeds were higher than those of the grape peels (p < 0.001). Both of the TFC values of the grape peels and seeds were lower than those of most medicinal plants and some common plant/tree waste [51,52]. Moreover, extracts with higher TPC values did not always have higher TFC values, different extracts contained different levels of TFC as a portion of phenols [51,52,53]. So it should be pointed out that grape peels and seeds were valuable resources of natural phenols but not flavonoids.

2.5. Correlations between Total FRAP, TEAC, TPC and TFC Values

The correlations between FRAP, TEAC, TPC and TFC values (based on the total values of three fractions) were detected using a simple linear regression model, and the results were displayed in Figure 1 and Figure 2.

Figure 1.

Figure 1

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Correlations between FRAP values and TPC values (A); FRAP values and TFC values (B); TEAC values and TPC values (C); TEAC values and TFC values (D); FRAP values and TEAC values (E); TPC values and TFC values (F) of peels from 30 grape varieties.

Figure 2.

Figure 2

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Correlations between FRAP values and TPC values (A); FRAP values and TFC values (B); TEAC values and TPC values (C); TEAC values and TFC values (D); FRAP values and TEAC values (E); TPC values and TFC values (F) of seeds collected from 10 grape varieties.

For grape peels, as seen from Figure 1, FRAP values and TEAC values were highly correlated to TPC values (R² = 0.865, p < 0.001 and R² = 0.892, p < 0.001, respectively), and moderately correlated to TFC values (R² = 0.760, p < 0.001 and R² = 0.732, p < 0.001, respectively). The outcomes revealed that phenolic components could be the main ingredients responsible for the antioxidant capacities of the grape peels, and flavonoid compounds might contribute to the antioxidant capacities of grape peels but were not the main contributors. In addition, TPC values were weakly correlated with TFC values (R² = 0.596, p < 0.001). It suggested that flavonoids comprised only a small part of phenolic components of the grape peels. Furthermore, FRAP values were significantly correlated with TEAC values (R² = 0.970, p < 0.001), so the antioxidant ingredients in the grape peels could reduce oxidants (like Fe(III)) and scavenge free radicals (like ABTS•+).

For grape seeds, according to Figure 2, FRAP values and TEAC values were intensely correlated to TPC values (R² = 0.993, p < 0.001 and R² = 0.945, p < 0.001, respectively), but not correlated to TFC values (R² = 0.007, p = 0.825 and R² = 0.041, p = 0.574, respectively). The outcomes suggested that phenolic components could be the main contributors to the antioxidant capacities of the grape seeds, but flavonoid compounds had little influence on the antioxidant capacities of grape seeds. Additionally, there was no linear correlation between TPC values and TFC values (R² = 0.010, p = 0.779), which suggested that phenolic components of the grape seeds were rarely flavonoids. Moreover, the correlation between FRAP values and TEAC values was remarkable (R² = 0.935, p < 0.001), so the antioxidant components in these grape seeds could also reduce oxidants (like Fe(III)) and scavenge free radicals (like ABTS•+).

The results illustrated above are consistent with many previous studies, which have reported that phenolic components were the main contributors responsible for the antioxidant capacities, and could reduce oxidants and scavenge free radicals [31,33,34,35,36]. On the contrary, these results were quite different from some other studies that reported a very weak correlation (R2 = 0.0337) between the FRAP values and TEAC values [32,37], indicating that the ingredients possessing reducing activities and those possessing free radicals scavenging activities in the 62 fruits were not the same, and a very weak correlation (R2 = 0.0404) between the TEAC values and TPC values, suggesting that phenolic components could not be the main contributors to the free radicals scavenging abilities of the 62 fruits. Li et al. [37] also reported a very weak correlation between the TEAC values and the FRAP values (R2 = 0.1563) as well as the FRAP values and the TPC values (R2 = 0.1966), which suggested that phenolic components could not be the main contributors to activities of the 223 medicinal plants to reduce oxidants.

2.6. Phenolic Components of the Grape Peels and Seeds

Phenolic components of the grape peels and seeds were determined on the base of the literature reported by Cai et al. with small alteration [54]. Phenolic components of the grape peels and seeds were detected, and the results were displayed in Table 5. Furthermore, the chromatograms under 220 nm of the mixed standards and the samples of Black Grape (Yunnan, China) peel and Pearl Black Grape (Xinjiang, China) seed were shown in Figure 3.

Table 5.

Phenolic components of peels and seeds from 30 grape varieties.

Name of Grapes Place of Production Part of Grapes Phenols Total Contents (mg/g FW)
Black Grape Yunnan, China Peel cyanidin-3-glucoside 0.174 ± 0.009
ferulaic acid 0.241 ± 0.011
rutin 0.073 ± 0.006
resveratrol 0.266 ± 0.015
Blackcurrant Grape California, CA, USA Peel cyanidin-3-glucoside 0.498 ± 0.028
rutin 0.687 ± 0.047
Flame Grape Xinjiang, China Peel cyanidin-3-glucoside 0.421 ± 0.023
ferulaic acid 0.049 ± 0.003
rutin 0.367 ± 0.015
Fragrant Green Grape Yunnan, China Peel rutin 0.383 ± 0.019
Golden Finger Grape California, CA, USA Peel cyanidin-3-glucoside 0.150 ± 0.007
ferulaic acid 0.041 ± 0.003
rutin 0.569 ± 0.034
Green Grape Victoria, Australia Peel rutin 0.268 ± 0.025
Ito Kyoho Grape Yunnan, China Peel epicatechin 0.015 ± 0.001
rutin 0.035 ± 0.003
Kyoho Grape Liaoning, China Peel rutin 0.113 ± 0.005
Kyoho Grape Xinjiang, China Peel epicatechin 0.026 ± 0.002
rutin 0.129 ± 0.009
Kyoho Grape Guangxi, China Peel rutin 0.138 ± 0.008
Kyoho Grape Yunnan, China Peel rutin 0.117 ± 0.006
Pearl Black Grape Xinjiang, China Peel rutin 0.199 ± 0.007
Pearl Green Grape Xinjiang, China Peel rutin 0.016 ± 0.000
Pearl Green Grape Victoria, Australia Peel rutin 0.047 ± 0.002
Red Grape Yunnan, China Peel cyanidin-3-glucoside 0.326 ± 0.023
rutin 0.804 ± 0.055
Red Grape Guangxi, China Peel cyanidin-3-glucoside 0.211 ± 0.007
rutin 0.293 ± 0.026
Red Grape Xinjiang, China Peel cyanidin-3-glucoside 0.412 ± 0.033
rutin 0.298 ± 0.027
Red Grape California, China Peel cyanidin-3-glucoside 0.377 ± 0.030
rutin 0.298 ± 0.020
Rose Black Grape Xinjiang, China Peel rutin 0.137 ± 0.006
Rose Black Grape Yunnan, China Peel rutin 0.030 ± 0.001
Seedless Black Grape Xinjiang, China Peel rutin 0.059 ± 0.002
Seedless Black Grape California, CA, USA Peel rutin 0.265 ± 0.022
Seedless Dew Grape Xinjiang, China Peel rutin 0.049 ± 0.001
Seedless Green Grape Xinjiang, China Peel rutin 0.008 ± 0.000
Seedless Red Grape Yunnan, China Peel rutin 0.176 ± 0.012
Seedless Red Grape Xinjiang, China Peel cyanidin-3-glucoside 0.021 ± 0.001
rutin 0.195 ± 0.013
Seedless Red Grape California, CA, USA Peel cyanidin-3-glucoside 0.058 ± 0.003
rutin 0.666 ± 0.056
Seedless Red Grape Victoria, Australia Peel cyanidin-3-glucoside 0.272 ± 0.011
rutin 0.594 ± 0.036
Summer Black Grape Shaanxi, China Peel epicatechin 0.051 ± 0.004
rutin 0.150 ± 0.006
Summer Black Grape Xinjiang, China Peel rutin 0.125 ± 0.003
Black Grape Yunnan, China Seed gallic acid 0.146 ± 0.008
cyanidin-3-glucoside 0.305 ± 0.028
epicatechin 1.207 ± 0.074
catechin gallate 0.052 ± 0.002
Ito Kyoho Grape Yunnan, China Seed gallic acid 0.054 ± 0.003
cyanidin-3-glucoside 0.840 ± 0.052
epicatechin 1.693 ± 0.094
catechin gallate 0.028 ± 0.002
Kyoho Grape Xinjiang, China Seed gallic acid 0.066 ± 0.003
cyanidin-3-glucoside 0.180 ± 0.011
epicatechin 2.088 ± 0.106
catechin gallate 0.119 ± 0.004
Kyoho Grape Guangxi, China Seed gallic acid 0.052 ± 0.002
cyanidin-3-glucoside 0.105 ± 0.005
epicatechin 2.039 ± 0.187
catechin gallate 0.044 ± 0.002
Kyoho Grape Yunnan, China Seed gallic acid 0.087 ± 0.002
cyanidin-3-glucoside 0.202 ± 0.019
epicatechin 1.886 ± 0.165
catechin gallate 0.054 ± 0.002
Pearl Black Grape Xinjiang, China Seed gallic acid 0.193 ± 0.017
cyanidin-3-glucoside 0.189 ± 0.009
epicatechin 1.745 ± 0.111
catechin gallate 0.126 ± 0.005
Red Grape Yunnan, China Seed gallic acid 0.236 ± 0.009
cyanidin-3-glucoside 0.113 ± 0.003
epicatechin 2.156 ± 0.156
catechin gallate 0.176 ± 0.008
Red Grape Guangxi, China Seed gallic acid 0.089 ± 0.004
cyanidin-3-glucoside 0.095 ± 0.005
epicatechin 1.547 ± 0.144
catechin gallate 0.145 ± 0.005
Red Grape Xinjiang, China Seed gallic acid 0.056 ± 0.002
cyanidin-3-glucoside 0.058 ± 0.003
epicatechin 1.644 ± 0.098
catechin gallate 0.128 ± 0.004
Red Grape California, CA, USA Seed gallic acid 0.022 ± 0.001
cyanidin-3-glucoside 0.111 ± 0.005
epicatechin 0.877 ± 0.065
catechin gallate 0.165 ± 0.013
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Figure 3.

Figure 3

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Chromatograms under 220 nm of the standard compounds (A); Black Grape (Yunnan, China) peel (B); Pearl Black Grape (Xinjiang, China) seed (C).The numbers in brackets refer to the compounds: gallic acid (1); protocatechuic acid (2); gallo catechin (3); chlorogenic acid (4); cyanidin-3-glucoside (5); caffeic acid (6); epicatechin (7); catechin gallate (8); p-coumaric acid (9); ferulaic acid (10); melatonin (11); 2-hydroxycinnamic acid (12); rutin (13); resveratrol (14); daidzein (15); equol (16); quercetin (17); genistein (18).

As seen from Table 5, five phenols, including cyanidin-3-glucoside, epicatechin, rutin, ferulaic acid and resveratrol, were found in the 30 grape peels. Every grape peel sample contained rutin, and the contents ranged from 0.008 ± 0.000 to 0.804 ± 0.055 mg/g FW with a 100-fold difference. The peel of Red Grape (Yunnan, China) possessed the highest level of rutin. Some grape peels contained cyanidin-3-glucoside, and the contents ranged from 0.021 ± 0.001 to 0.498 ± 0.028 mg/g FW with a 24-fold difference. The peel of Blackcurrant Grape (California, CA, USA) possessed the highest level of cyanidin-3-glucoside. The peels of Summer Black Grape (Shaanxi, China), Kyoho Grape (Xinjiang, China) and Ito Kyoho Grape (Yunnan, China) contained epicatechin of 0.051 ± 0.004, 0.026 ± 0.002 and 0.015 ± 0.001 mg/g FW, and the peels of Black Grape (Yunnan, China), Flame Grape (Xinjiang, China) and Golden Finger Grape (California, CA, USA) contained ferulaic acid of 0.241 ± 0.011, 0.049 ± 0.003 and 0.041 ± 0.003 mg/g FW, while resveratrol (0.266 ± 0.015 mg/g FW) was only detected in the peel of Black Grape (Yunnan, China).

As for the 10 grape seeds, four phenols including gallic acid, cyanidin-3-glucoside, epicatechin and catechin gallate were found in all of them, and the content ranges were as follows, respectively: 0.022 ± 0.001 to 0.236 ± 0.009 mg/g FW with a 10-fold difference; 0.058 ± 0.003 to 0.840 ± 0.052 mg/g FW with a 14-fold difference; 0.877 ± 0.065 to 2.156 ± 0.156 mg/g FW with a 2-fold difference; 0.028 ± 0.002 to 0.176 ± 0.008 mg/g FW with a 7-fold difference, respectively. The seeds of Red Grape (Yunnan, China), Ito Kyoho Grape (Yunnan, China), Red Grape (Yunnan, China) and Red Grape (Yunnan, China) possessed the highest level of gallic acid, cyanidin-3-glucoside, epicatechin and catechin gallate, respectively. These results also prove our hypothesis that grapes with diverse genotypes have different composition and contents of bioactive compounds. Furthermore, it was reported that phenols like cyanidin-3-glucoside, resveratrol and rutin possessed varies bioactivities, such as antibacterium, antioxidant, anti-inflammation and hepatic and cardiovascular protection, so grape peels and seeds from juice and wine industries could be valuable resources to extract phenols with further use in producing functional foods, food additives and pharmaceuticals.

The above results were expressed on the weight of fresh material. In addition, the moisture contents of the grape peels and seeds are displayed in Table 6, which could be used to express the results on the weight of dry material.

Table 6.

Moisture contents of the tested grape peels and seeds.

Name of Grapes Place of Production Part of Grapes Moisture Contents (%)
Black Grape Yunnan, China Peel 72.333 ± 2.951
Blackcurrant Grape California, CA, USA Peel 72.382 ± 1.023
Flame Grape Xinjiang, China Peel 58.699 ± 2.487
Fragrant Green Grape Yunnan, China Peel 74.926 ± 3.156
Golden Finger Grape California, CA, USA Peel 71.851 ± 2.894
Green Grape Victoria, Australia Peel 79.027 ± 0.525
Ito Kyoho Grape Yunnan, China Peel 77.103 ± 3.446
Kyoho Grape Guangxi, China Peel 77.402 ± 1.568
Kyoho Grape Liaoning, China Peel 80.564 ± 3.699
Kyoho Grape Xinjiang, China Peel 78.757 ± 3.321
Kyoho Grape Yunnan, China Peel 79.920 ± 3.219
Pearl Black Grape Xinjiang, China Peel 79.023 ± 3.013
Pearl Green Grape Xinjiang, China Peel 74.881 ± 0.856
Pearl Green Grape Victoria, Australia Peel 75.233 ± 3.112
Red Grape California, CA, USA Peel 76.320 ± 3.239
Red Grape Guangxi, China Peel 77.416 ± 2.986
Red Grape Xinjiang, China Peel 73.806 ± 2.357
Red Grape Yunnan, China Peel 76.117 ± 2.766
Rose Black Grape Xinjiang, China Peel 69.404 ± 2.551
Rose Black Grape Yunnan, China Peel 69.726 ± 0.469
Seedless Black Grape California, CA, USA Peel 72.423 ± 2.995
Seedless Black Grape Xinjiang, China Peel 69.200 ± 2.210
Seedless Dew Grape Xinjiang, China Peel 74.168 ± 2.848
Seedless Green Grape Xinjiang, China Peel 72.232 ± 2.365
Seedless Red Grape California, CA, USA Peel 71.103 ± 1.334
Seedless Red Grape Victoria, Australia Peel 66.384 ± 2.085
Seedless Red Grape Xinjiang, China Peel 73.000 ± 2.462
Seedless Red Grape Yunnan, China Peel 73.293 ± 2.366
Summer Black Grape Shaanxi, China Peel 71.560 ± 2.232
Summer Black Grape Xinjiang, China Peel 69.450 ± 2.211
Black Grape Yunnan, China Seed 42.396 ± 1.845
Ito Kyoho Grape Yunnan, China Seed 44.002 ± 1.933
Kyoho Grape Xinjiang, China Seed 41.664 ± 0.759
Kyoho Grape Guangxi, China Seed 43.489 ± 1.926
Kyoho Grape Yunnan, China Seed 44.001 ± 1.988
Pearl Black Grape Xinjiang, China Seed 46.646 ± 2.003
Red Grape Yunnan, China Seed 52.859 ± 2.109
Red Grape Guangxi, China Seed 51.622 ± 0.221
Red Grape Xinjiang, China Seed 46.424 ± 1.903
Red Grape California, CA, USA Seed 51.570 ± 2.158
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3. Materials and Methods

3.1. Chemical Reagents

The 2,2′-azinobis(3-ethylbenothiazoline-6-sulphonic acid) diammonium salt (ABTS), 6-hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic acid (Trolox), 2,4,6-tri(2-pyridyl)-s-triazine (TPTZ), Folin-Ciocalteu’s phenol reagent, and the standard compounds (gallic acid, protocatechuic acid, gallo catechin, chlorogenic acid, cyanidin-3-glucoside, caffeic acid, epicatechin, catechin gallate, p-coumaric acid, ferulaic acid, melatonin, 2-hydroxycinnamic acid, rutin, resveratrol, daidzein, equol, quercetin and genistein) were provided by Sigma-Aldrich (St. Louis, MO, USA). Tetrahydrofuran, methanol, formic acid, diethyl ether and ethyl acetate were provided by Kermel Chemical Factory (Tianjin, China). Acetic acid, sodium acetate, potassium acetate, sodium hydroxide, hydrochloric acid, ethylenediaminetetraacetic acid (EDTA), ascorbic acid, iron (III) chloride hexahydrate (FeCl3·6H2O), iron(II) sulphate heptahydrate (FeSO4·7H2O), potassium persulphate, sodium carbonate, aluminum chloride hexahydrate (AlCl3·6H2O), ethanol and n-hexane were provided by Damao Chemical Factory (Tianjin, China). All chemical reagents used in the tests were of analytical or chromatographic grade, and the water used was double distilled.

3.2. Sample Preparation

Grapes from 30 varieties produced in China, USA and Australia (Figure 4) were obtained from local shops in Guangzhou, China. Grapes were washed with double distilled water and dried at room temperature. The grapes were separated into peels, pulps and seeds, and then the peels and seeds were respectively ground into particles using a special grinder for food processing. After that, accurate 2.000 g of the samples were weighed and extracted with 10 mL tetrahydrofuran at 30 °C for 30 min in a shaking water bath [55]. The samples were centrifuged at 4200 g for 10 min, and the supernatants were gathered. The extraction was repeated twice, and the supernatants were collected as the fat-soluble fractions. Subsequently, the residues were extracted with 10 mL methanol-acetic acid-water (50:3.7:46.3, v/v/v) mixture at 30 °C for 30 min in a shaking water bath, which was also repeated twice, and the supernatants were gathered up as the water-soluble fractions. Furthermore, the residues were hydrolyzed with 5 mL sodium hydroxide solution (2 mol/L NaOH, 10 mmol/L EDTA, 1% ascorbic acid) at 37 °C for 30 min in a shaking water bath, and then acidified to pH = 2 with 6 mol/L hydrochloric acid solution [56]. The mixtures were extracted twice with 5 mL n-hexane to eliminate fatty acids, which might be released during alkaline hydrolysis. Immediately, the mixtures were extracted twice with 5 mL diethyl ether and ethyl acetate mixture (1:1, v/v), and the organic phases were collected. The extracts were dried out at room temperature under a stream of N2 using an evaporator and reconstituted in ethanol as the insoluble-bound fractions. All extracts were preserved at −20 °C until tested.

Figure 4.

Figure 4

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Coordinates of geographical areas of the tested grapes.

3.3. FRAP Assay

The FRAP assay was conducted referring to the literature with minor alterations [27]. Briefly, the FRAP reagent was a mixture of 300 mmol/L sodium acetate-acetic acid buffer (pH = 3.6), 10 mmol/L TPTZ solution (40 mmol/L hydrochloric acid solution as solvent) and 20 mmol/L FeCl3 solution (10:1:1, v/v/v), and it was prepared freshly and warmed to 37 °C in a water bath before used. The 0.1 mL properly diluted sample was combined with 3 mL FRAP reagent. After incubated at room temperature for 4 min, a CANY 722 visible spectrophotometer (Shanghai, China) was used to measure the absorbance of the mixtures at 593 nm. The size and volume of cuvette were 1 cm × 1 cm × 4.5 cm and 4.5 mL, respectively. The assay volumes were 1/2 to 2/3 of the volume of cuvette. The results were expressed as μmol Fe (II)/g FW of the grape peels or seeds.

3.4. TEAC Assay

The TEAC assay was carried out according to the literature with minor alterations [41]. Accordingly, the ABTS•+ stock solution was a mixture of 7 mmol/L ABTS solution and 2.45 mmol/L potassium persulphate solution (1:1, v/v), which was incubated in the dark for at least 16 h at room temperature and used within 2 days. The ABTS•+ working solution was obtained by diluting the stock solution with ethanol to an absorbance of 0.710 ± 0.05 at 734 nm. The samples were diluted approximately until they can inhibit 20–80% blank absorbance. Subsequently, the 0.1 mL properly diluted sample was mixed with 3.8 mL ABTS•+ working solution and measured at 734 nm after incubated at room temperature for 6 min. The percent of inhibition of absorbance was calculated to evaluate of the antioxidant capacity. The results were expressed as μmol Trolox/g FW of the grape peels or seeds.

3.5. Determination of TPC

The TPC values were determined based on procedures reported by Singleton, Orthofer and Lamuela-Raventos [49]. Briefly, a properly diluted sample (0.5 mL) was added to Folin-Ciocalteu reagent (0.2 mol/L, 2.5 mL). After 4 min, saturated sodium carbonate solution (about 75 g/L, 2 mL) was added to the mixture. The mixture was incubated at room temperature for 2 h, and then the absorbance was measured at 760 nm. The results were expressed as milligram gallic acid equivalent (mg GAE)/g FW of the grape peels or seeds.

3.6. Determination of TFC

The TFC values were determined according to the literature reported by Kalia et al. [50]. Accordingly, a properly diluted sample (0.5 mL) was mixed with ethanol solution (95%, v/v, 1.5 mL), AlCl3 solution (10%, w/v, 0.1 mL), potassium acetate solution (1 mol/L, 0.1 mL) and double distilled water (2.8 mL). The mixture was incubated for 30 min at room temperature, and then the absorbance was measured at 415 nm. The results were expressed as mg quercetin equivalent (mg QE)/g FW of the grape peels or seeds.

3.7. HPLC Analysis

The phenolic and flavonoid components in the samples were detected by HPLC-PDAD (photodiode array detector) based on the method reported by Cai et al. with small modifcations [54]. In detail, the HPLC system included a Waters (Milford, MA, USA) 1525 binary HPLC pump separation module with an auto-injector and employed a Waters 2996 PDAD. Separation was carried out with an Agilent Zorbax Extend-C18 column (250 × 4.6 mm, 5 μm) at 40 °C with a gradient elution solution A, composed of formic acid solution (0.1%, v/v), and solution B, methanol, which were routinely delivered at a flow rate of 0.8 mL/min according to the procedure: 0 min, 95% (A); 15 min, 80% (A); 20 min, 70% (A); 25 min, 63% (A); 40 min, 60% (A); 60 min, 50% (A); 65 min, 50% (A); 65.1 min, 95% (A); and 70 min, 95% (A). Fat-soluble, water-soluble and insoluble-bound fractions were combined together before sampling. The spectra were recorded between 200 and 600 nm to characterize the peak patterns. Phenolic and flavonoid components were identified by the retention time and UV-Vis spectra comparing with standards and quantified by the peak area under maximum absorption wavelength, and the results were expressed as mg/g FW of the grape peels or seeds.

3.8. Data Analysis

All tests were conducted in triplicate and the values were expressed as mean ± SD (standard deviation). Data analysis was performed using SPSS 22 (International Business Machines Corporation, Armonk, NY, USA) and Excel 2007 (Microsoft Corporation, Redmond, WA, USA).

4. Conclusions

In this study, the antioxidant capacities and total phenolic and flavonoid contents of peels and seeds from 30 grape varieties were systematically evaluated. The antioxidant capacities and phenolic and flavonoid contents of the grape peels and seeds were greatly different, and those of the three fractions were, in decreasing order: fat-soluble fractions > water-soluble fractions > insoluble-bound fractions. Antioxidant components in these grape peels and seeds could reduce oxidants and scavenge free radicals, and phenols were the main contributors to the antioxidant capacities, and flavonoids were not major contributors to these activities. Several phenolic compounds such as gallic acid, cyanidin-3-glucoside, epicatechin, catechin gallate, ferulaic acid, rutin and resveratrol were identified and quantified in these grape peels and seeds. These grape wastes could be abundant sources of natural bioactive compounds for developing functional foods, food additives and pharmaceuticals.

Acknowledgments

We acknowledge Dr. Qin Xiao for technical support.

Author Contributions

Conceptualization, G.-Y.T., S.L. and H.-B.L.; Methodology, G.-Y.T. and C.-N.Z.; Software, Q.L.; Validation, G.-Y.T.; Formal Analysis, C.-N.Z.; Investigation, G.-Y.T., C.-N.Z., Q.L., X.-L.F., X.-Y.X., S.-Y.C. and X.M.; Resources, G.-Y.T.; Data Curation, C.-N.Z.; Writing-Original Draft Preparation, G.-Y.T.; Writing-Review & Editing, S.L., R.-Y.G. and H.-B.L.; Visualization, G.-Y.T.; Supervision, H.-B.L.; Project Administration, H.-B.L.; Funding Acquisition, R.-Y.G. and H.-B.L.

Funding

This work was supported by the Shanghai Pujiang Talent Plan (No. 18PJ1404600); Shanghai Basic and Key Program (No. 18JC1410800); National Natural Science Foundation of China (No. 81372976); Key Project of Guangdong Provincial Science and Technology Program (No. 2014B020205002); and the Hundred-Talents Scheme of Sun Yat-Sen University.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Sample Availability: Samples of the compounds are unavailable from the authors.

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