Article pubs.acs.org/JAFC
Quantification and Bioaccessibility of California Pistachio Bioactives Yuntao Liu,†,‡ Jeffrey B. Blumberg,† and C.-Y. Oliver Chen*,† †
Antioxidants Research Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, 711 Washington Street, Boston, Massachusetts 02111, United Stated ‡ State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi 214122, China S Supporting Information *
ABSTRACT: The content of carotenoids, chlorophylls, phenolics, and tocols in pistachios (Pistacia vera L.) has not been methodically quantified. The objective of this study was to first optimize extraction protocols for lipophilic nutrients and then quantify the content of two phenolic acids, nine flavonoids, four carotenoids, two chlorophylls, and three tocols in the skin, nutmeat, and whole nut of California pistachios. The dominant bioactives in whole pistachios are lutein [42.35 μg/g fresh weight (FW)], chlorophyll a (142.24 μg/g FW), γ-tocopherol (182.20 μg/g FW), flavan-3-ols (catechins) (199.18 μg/g FW), luteolin (217.89 μg/g FW), myricetin (135.18 μg/g FW), and cyanidin-3-galactose (38.34 μg/g FW) in each nutrient class. Most phenolics are present in the skin, while the lipophilic nutrients are dominantly present in the nutmeat. Digestion with a gastrointestinal mimic showed chlorophyll a > chlorophyll b > lutein > α-tocopherol > γtocotrienol > β-carotene > zeaxanthin > α-carotene. The concentration of α-tocopherol and γ-tocotrienol were at least 81% lower than that of γ-tocopherol. While all nine compounds were detected in pistachio skins, their contribution to whole pistachios was minimal, ranging from 5.3% for α-carotene to 0.1% for chlorophyll A. The calculated sum of each lipophilic compound in the skin (6%) and the nutmeat (94%) was 21 ± 8% lower than the value obtained in whole pistachios, ranging from 4% (α-carotene) to 31% (chlorophyll a).
Figure 3. The effect of solvent on the extraction efficiency of esterified lipophilic bioactives. Means bearing different letter within each nutrient differ (n = 3); P < 0.05, tested by one-way ANOVA, followed by the HSD Tukey’s test.
comparable efficiency and were ≥38.5 and 62.7% larger than MTBE, respectively (P < 0.05). As hexane extracted slightly more of these two compounds than diethyl ether, hexane was selected for the study. Optimal Extraction Condition for Chlorophylls. Anhydrous Na2CO3 has been employed in the extraction of chlorophylls to prevent their conversion to pheophytins.19 The addition of Na2CO3 to methanol decreased the amount of extractable chlorophylls as compared to methanol alone (Figure 4A,B) C
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Table 1. Content (μg/g FW) of Carotenoids, Chlorophylls, and Tocopherols in Skins, Nutmeat, and Whole Nutsa bioactives
skins (GI)b
skins
α-carotene β-carotene lutein zeaxanthin
0.26 1.24 4.17 0.76
± ± ± ±
chlorophyll a chlorophyll b
4.59 ± 0.28 (0.1%) a 2.26 ± 0.20 (0.4%) a
ND ND
α-tocopherol γ-tocopherol γ-tocotrienol
22.02 ± 2.28 (5%) a 42.14 ± 9.34 (1.6%) b 6.23 ± 0.22 (3%) a
ND ND ND
0.02 0.08 0.24 0.03
(5.3%)d a (3.3%) a (0.8%) a (5.5%) a
NDc ND ND ND
nutmeat
nutmeat (GI)
Carotenoids 0.29 ± 0.02 a 2.34 ± 0.12 b 35.43 ± 3.36 b 0.98 ± 0.09 a Chlorophylls 104.28 ± 10.76 b 34.78 ± 3.76 b Tocols 26.51 ± 0.87 b 165.72 ± 14.09 c 12.67 ± 1.19 b
whole nuts
whole nuts (GI)
ND ND 2.61 ± 0.11 a ND
0.30 ± 0.04 a 2.94 ± 0.24 c 42.35 ± 5.88 b 1.66 ± 0.20 b
ND ND 2.80 ± 0.11 a ND
ND ND
142.24 ± 20.78 c 44.74 ± 6.49 c
ND ND
ND 7.42 ± 0.52 a ND
34.26 ± 2.02 c 182.20 ± 24.67 c 16.68 ± 2.50 c
ND 9.65 ± 0.48 ab ND
Results are expressed as mean ± SD, n = 3. Means bearing different letters within a row differ; P < 0.05, tested by one-way ANOVA, followed by the HSD Tukey’s test. bGI: gastrointestinal digestion mimic. cND: not detected. dThe percent contribution of the bioactives in the skins to those in whole nuts was calculated on the basis of the following equation: (amount of bioactives in skins × 0.06)/[(amount of bioactives in nutmeat × 0.94) + (the amount of bioactives in skins × 0.06)] × 100%. a
Table 2. Content (μg/g FW) of Phenolics in Skins, Nutmeat, and Whole Nutsa bioactives gallic acid protocatechuic acid catechin epicatechin rutin eriodictyol total quercetin quercetin (M)e quercetin (H)f total luteolin luteolin (M) luteolin (H) total myricetin myricetin (M) myricetin (H) cyanidin-3-galactoside cyanidin 3-glucoside
skins 197.4 ± 14.1 (51.2%) e 90.0 ± 7.4 (71.1%) f 1774.2 ± 74.2 (84.0%) e 229.1 ± 15.5 (100%) d 57.6 ± 3.4 (100%) b 59.2 ± 2.5 (100%) d 144.4 ± 10.4 (41.4%) c 43.4 ± 0.9 b 101.0 ± 9.8 c 52.8 ± 2.5 (2%) a 37.3 ± 1.6 b 15.4 ± 3.3 a 68.2 ± 4.7 (3.0%) a ND 68.2 ± 2.6 a 876.5 ± 52.1 (100%) d 212.7 ± 17.7 (100%) d d
skins (GI)b
nutmeat
nutmeat (GI)
whole nuts
136.8 ± 7.2 e 46.7 ± 2.9 e 324.7 ± 43.7 d 57.1 ± 4.7 c 15.3 ± 1.2 a 16.1 ± 0.6 b 8.1 ± 0.8 a − − ND − − ND − − 77.7 ± 5.7 c 23.8 ± 1.4 c
11.9 ± 2.8 c 2.3 ± 0.1 b 21.5 ± 0.6 b ND ND ND 13.0 ± 1.0 a ND 13.0 ± 1.0 a 204.9 ± 5.3 b ND 204.9 ± 5.3 b 140.6 ± 3.3 b ND 140.6 ± 3.3 b ND ND
0.44 ± 0.04 a 0.92 ± 0.10 a NDc ND ND ND ND − − ND − − ND − − ND ND
36.5 ± 1.4 d 14.0 ± 0.5 d 199.2 ± 22.2 c 26.2 ± 2.6 b ND 26.3 ± 2.6 c 43.5 ± 1.7 b 4.7 ± 0.0 a 38.8 ± 1.7 b 217.9 ± 6.1 b 5.8 ± 1.1 a 212.1 ± 5.8 b 135.2 ± 5.4 b − 135.2 ± 5.4 b 38.3 ± 2.2 b 9.2 ± 1.5 b
whole nuts (GI) 3.3 ± 4.8 ± 4.7 ± 1.1 ± ND 1.0 ± ND − − ND − − ND − − 1.2 ± 0.5 ±
0.1 0.6 0.3 0.1
b c a a
0.0 a
0.1 a 0.0 a
a Results are expressed as mean ± SD, n = 3. Means bearing different letters within a row differ; P < 0.05, tested by one-way ANOVA, followed by the HSD Tukey’s test. bGI: gastrointestinal digestion mimic. cND: not detected. dThe percent contribution of the bioactives in the skin to those in whole nuts was calculated on the basis of the following equation: (amount of bioactives in skin × 0.06)/[(amount of bioactives in nutmeat × 0.94) + (the amount of bioactives in skin ×0.06)] × 100%. eM: Concentration obtained after acidified methanol extraction. fH: Concentration obtained after acid hydrolysis treatment.
rutin, eriodictyol, cyanidin-3-galactoside, and cyanidin-3-glucoside. The glycon form of quercetin, luteolin, and myricetin was quantified after the acidified hydrolysis. Myricetin was present exclusively as the glycone form in the skins and nutmeat. Quercetin and luteolin were found in the glycon form in the nutmeat and were present as the glycon and aglycon in the skins. The calculated sum of each nonanthocyanin compound in the skins (6%) and the nutmeat (94%) was 40 ± 24% lower than the value in whole pistachios, ranging from 1% (myricetin) to 86% (eriodictyol). The calculated sum of cyanidin-3galactoside and cyanidin-3-glucoside was 37 and 39% larger than their value obtained in whole pistachios, respectively. With the in vitro GI mimic digestion, only gallic and protocatechuic acids were detected, with their concentration ≤1 μg/g in the nutmeat. In the skins, except for luteolin and myricetin, the other nine compounds were all detected with their concentration being 30−94% lower than the corresponding value found in the acidified methanol extract. Only seven
We employed the in vitro GI mimic digestion mimic to estimate the bioaccessibility of the lipophilic nutrients. As the efficiency of the extraction appeared low for lipophilic compounds, these nutrients were not detected in the skin. Only lutein and γ-tocopherol were quantifiable in the GI mimic extract of nutmeat and whole pistachios. Their concentrations were 93 and 95% lower than those quantified after the extraction using the organic solvents described above. Quantification of Phenolics in Pistachios. Eleven phenolic compounds were detected and quantified in pistachios (Table 2). All 11 compounds were detected in the skin, but only 6 were found in the nutmeat. The dominant phenolics in the skins with the concentration ≥100 μg/g FW were catechin, cyanidin-3-galactoside, epicatechin, cyanidin-3-glucoside, gallic acid, and quercetin, in descending order. The nutmeat was rich in luteolin and myricetin, with concentrations ≥140 μg/g. The percentage contribution of the phenolics in the skins to whole pistachios ranged from 2% for luteolin to 100% for epicatechin, D
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cyanidin-3-galactoside, catechin, quercetin, luteolin, and myricetin, with their content being ≥38 μg/g FW. Interestingly, the calculated sum of each compound in the skins and nutmeat was generally lower than that quantified in whole pistachios. We speculate the difference was attributed to the reciprocal protection of antioxidants in pistachios against degradation during the extraction and the storage before analysis. γ-Tocopherol is the dominant tocol in pistachios.3,9,24 Consistent to the literature, we found γ-tocopherol is the main tocol in California pistachios, followed by α-tocopherol and γ-tocotrienol. Kornsteiner et al. reported that δ-tocopherol was detected at a concentration of 5 μg/g FW, while αtocopherol was not detected.24 However, Mandalari et al. found all three forms.9 The α- and γ-tocopherol content of pistachios has been reported to range from 0 to 11 and 105 to 293 μg/g FW, respectively.2,9,24 The content of γ-tocopherol [182.2 μg/g fresh weight (FW)] found in our study is within this range, while α-tocopherol (34.3 μg/g FW) is about 2-fold larger. The well-appreciated factors determining phytochemical contents, including cultivar, harvest season, cultivation practice, irrigation, growing region, soil, maturity level, and postharvest processing, may all contribute to the difference in the tocol contents of pistachios, as well as other phytochemicals. Carotenoids are found in pistachios and other tree nuts with the exception of Brazil nuts and macadamias.33 We found αand β-carotene, lutein, and zeaxanthin mainly in the nutmeat of pistachios, as compared to lutein, violaxanthin, neoxanthin, luteoxanthin, and β-carotene reported by Giuffrida et al.34 The other three studies of pistachios reported only the presence of lutein and/or β-carotene.9,24,30 The reported content of βcarotene and lutein in pistachios ranges from 0 to 7 μg/g and 17 to 52 μg/g FW, respectively.2,9,24,30,34 The content of βcarotene (2.94 μg/g) and lutein (42.35 μg/g) found in this study are within these ranges. Chlorophylls are a conjugated tetrapyrrole ring that allows them to absorb light, thereby contributing to photosynthesis, color, and oxidative stability of plants.34 Chlorophylls may also play a role in human health due to their antioxidant and antimutagenic activities.35,36 Pistachios and pine nuts are the only two tree nuts containing chlorophylls.33 Chlorophyll a and b in pistachios harvested in Italy, Turkey, Greece, and Iran ranged from 18.3 to 150.6 and 7.1 to 49.7 μg/g, respectively.19,34 We found similar concentrations of chlorophyll in California pistachios. It is worth noting that Na2CO3 was employed in the extraction of chlorophylls in the studies by Bellomo and Fallico and Giuffrida et al.19,34 Our results establish an adverse effect of Na2CO3 on chlorophylls during extraction. Further, methanol is proved a better extraction solvent than the hexane and acetone/methanol (75:25) solvents used in these two studies, respectively.19,34 Thus, the chlorophyll contents reported in these studies might be underestimated. Pistachios contain a variety of phenolic compounds, e.g., anthocyanins, flavonols, and isoflavones.33 Consistent with a general understanding,30 we found pistachio phenolics are mainly present in the skins, with cyanidin-3-galactoside, catechin, quercetin, luteolin, and myricetin being the main compounds. According to the USDA flavonoid database, pistachios contain 68.5 μg/g flavanols, 14.6 μg/g flavonols, and 60.6 μg/g anthocyanins. While the content of anthocyanins in pistachios found in this study are 22% lower than the USDA value, the contents of flavanols and flavonols are 1.3- and 16.6fold larger. The main difference in flavonols is attributed to the
compounds were detected in whole pistachios after the GI mimic extraction. Their total content were ≤10% that obtained from the acidified methanol extraction. Gallic and protocatechuic acids and catechin were the main compounds liberated from whole pistachios during the GI mimic digestion.
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DISCUSSION A variety of low-polarity solvents has been employed for extraction of carotenoids, chlorophylls, and tocols in pistachios. Mandalari et al., Bellomo and Fallico, and Ballistreri et al. used hexane for carotenoids and tocopherols.9,19,20 Bellomo and Fallico employed acetone/methanol (75:25) for extraction of chlorophylls in pistachios, as compared to the study of Henriques et al. showing that methanol was the most suitable solvent for chlorophylls in marine microalga.19,21 Contrary to Mandalari et al., Bellomo and Fallico, and Ballistreri et al.,9,19,20 we found that methanol was superior to hexane and acetone/ methanol (75:25) for the extraction of chlorophylls and nonesterified γ-tocopherol. While hexane and methanol displayed comparable extraction efficiency for lutein in our study, Craft and Soares indicated that lutein was the least soluble in hexane among all tested organic solvents.22 As lutein is the dominant carotenoid in pistachios, we suggest that methanol is the most suitable solvent for extraction of nonesterified carotenoids and tocols and chlorophylls in pistachios. Anhydrous Na2CO3 has been added to the extraction solvents with the intention of preventing the conversion of chlorophylls to pheophytins.19 However, our results do not support the use of Na2CO3, in contrast to the reports from Bellomo et al. (for Italian pistachios) and Fuke et al. (for Kiwi fruit).19,23 In addition to the reduction in the extracted chlorophyll contents, Na2CO3 resulted in a lower recovery rate of lutein. Thus, the use of Na2CO3 for the maximum extraction efficiency for chlorophylls may depend on climate, soil, or genetic conditions of the cultivars. An adequate de-esterifying protocol is necessary to liberate esterified lipophilic bioactives to their free counterparts. On the basis of our results (data not shown), 62% of α-tocopherol in pistachios was present in the esterified form, as well as all αand β-carotene. The effectiveness of saponification to deesterify bioactives depends on incubation temperature and duration when the KOH concentration in methanol is fixed. There is a diversity of saponification conditions described in the literature, e.g., 30 min at 80 °C for 10 different nuts (including pistachios),24 10 min at 85 °C for soybeans,25 and 5 min at 50 °C for sausages,26 and 30 min at 70 °C for human serum and rat liver.27 We found that saponification at 60 °C for 30 min appears optimal for tocols and carotenoids in pistachios, which is slightly different from the conditions employed by Kornsteiner et al. for their analysis of nuts.24 Hexane, MTBE, and diethyl ether are usually employed as the extraction solvent of choice after the saponification.24,28,29 However, we found that hexane is the most suitable one for tocols and carotenoids. The phytochemical composition of pistachios has not been comprehensively examined for over 30 years,30 even though such information is important to understanding the mechanisms of action by which pistachio consumption may reduce the risk of cardiovascular disease.31 Consistent with the work of Tomaino et al.,32 we found that most lipophilic compounds exist in the nutmeat, while most hydrophilic compounds are present in the skins. The dominant compounds characterized in our study include γ-tocopherol, chlorophylls a and b, lutein, E
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tributed to study design, data interpretation, and manuscript preparation.
presence of myricetin. The wide variation is not unexpected, because phenolic contents in plant foods are subject to influence by growing location, season, cultivar, and food processing.6,9,10,20,32 In this study, we also tested in vitro bioaccessibility of pistachio bioactives in whole nuts using an upper GI mimic digestion protocol. It is worth noting that this protocol cannot fully reflect the mechanic and biochemical processes during human digestion. We observed that, as compared to the acidified methanol extraction, most phenolics found in pistachios were not readily accessible during the mimic digestion, with 5% phenolics being released, except protocatechuic and gallic acids. It is interesting to note that quercetin glycosides dominantly present in the skins were not released during the mimic digestion. As expected, fat-soluble nutrients in pistachios were not readily released to the aqueous GI mimic solvents, and only lutein and γ-tocopherol were found to be 90% accessible during an in vitro digestion using a more sophisticated system. Kay et al. reported in a dose−response trial that consumption of diets containing 10% (32−63 g/d) or 20% (64−126 g/d) daily calories from California pistachios for 4 weeks increased circulating β-carotene, lutein, and γtocopherol in hypercholesterolemic adults, suggesting bioavailability of the lipophilic bioactives. Thus, more clinical studies are needed to validate the bioaccessibility and bioavailability of other pistachio bioactives.37 Lipophilic bioactives, including four carotenoids, two chlorophylls, and three tocols, in California pistachios were methodically characterized, as their quantification was performed after extraction protocols were optimized with solvents, saponification condition, and Na2CO3 addition. Further, 11 hydrophilic bioactives (2 phenolic acids, 9 flavonoids) were characterized. The most dominant bioactives were lutein, chlorophyll a, γ-tocopherol, catechins, luteolin, myricetin, and cyanidin-3-galactose in each nutrient category. γTocotrienol, zeaxanthin, α-carotene, and myricetin were quantified in pistachios for the first time. California pistachios are good source of antioxidants, e.g., tocols, carotenoids, and phenolics. Thus, pistachios incorporated into healthy diets shall help enhance health by prevention of cancers and cardiovascular diseases. Bioactive contents in pistachios and other nuts shall be systematically assessed so that health benefits of nut consumption can be fully appreciated.
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Funding
This work was supported by the American Pistachio Growers and the U.S. Department of Agriculture (USDA)/Agricultural Research Service (Cooperative Agreement No. 58-1950-0-014). Notes
The contents of this publication do not necessarily reflect the views or policies of the USDA nor does mention of trade names, commercial products or organizations imply endorsement by the U.S. government. The authors declare no competing financial interest.
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ABBREVIATIONS USED MTBE, methyl tert-butyl ether; BHT, butylated hydroxytoluene; HPLC, high-performance liquid chromatography; LC− MS/MS, liquid chromatography−mass spectrometry/mass spectrometry; ECD, gastrointestinal mimic; GI, electrochemical detector.
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ASSOCIATED CONTENT
* Supporting Information S
Supplemental Table 1, a list of the content of free and esterified lipophilic bioactives in whole pistachios. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*Tel: 617-556-3128. Fax: 617-556-3344. E-mail: Oliver.Chen@ tufts.edu. Author Contributions
Y.L. conducted the experiments, performed statistical analysis, and prepared the manuscript. J.B.B. contributed to data interpretation and manuscript preparation. C.-Y.O.C. conF
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