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Article history: Elderberry industrial by-products can be a potential low cost source of some unique bioactive polyphe-
Received 21 May 2016 nols. Hence, the main objective of this work was to perform a comparative study of the polyphenol
Received in revised form 3 October 2016 profile of elderberry branches, the scavenging activity towards 2,2 -azino-bis(3-ethylbenzothiazoline)-
Accepted 9 October 2016
6-sulfonic acid, hydroxyl and nitric oxide radicals and to compare with those of the elderberry berries.
Available online 28 October 2016
Total phenolic compounds and anthocyanins were significantly higher in the berries when compared to
the branches (1.68 and 3.21 times, respectively), nevertheless the 2,2 -azino-bis(3-ethylbenzothiazoline-
Keywords:
6-sulfonic acid) and hydroxyl radicals scavenging activities were similar between the two materials, and
Elderberry
By-products
branches extract presented a higher nitric oxide radical scavenging activity. A total of 23 polyphenolic
Branches compounds were detected in all samples, of which thirteen compounds were present both in berries
Anthocyanins and branches, including cyanidin 3,5-diglucoside, cyanidin 3-sambubioside-5-glucoside, cyanidin 3-
Polyphenols glucoside and cyanidin 3-sambubioside. As elderberry production is increasing, as well the generation of
Antioxidant activity associated by products, the polyphenolic composition of the elderberry branches opens the possibility of
its valorization, using simple and relatively easy extraction procedures yielding extracts rich in polyphe-
nols possessing a significant antioxidant activity, useful to other emerging industrial and agricultural
applications.
© 2016 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.indcrop.2016.10.018
0926-6690/© 2016 Elsevier B.V. All rights reserved.
228 P. Silva et al. / Industrial Crops and Products 95 (2017) 227–234
for further industrial processing. The production of fresh refriger- 2013 in Varosa Valley, Portugal. Umbels were harvested from
ated elderberries generates a large amount of by-products, with four different points of tree, and the branches were removed
branches being the most abundant, accounting for more than 10% manually. Elderberry berries and branches were freeze-dried and
of the total elderberry production, being at present composted or milled in an electric mill, and then stored at −80 ◦ C until further
through away. During ripening of elderberry berries, especially in analysis. Representative voucher samples of elderberry branches
the last ripening stages, the branches acquire a distinct reddish and berries were deposited at the herbarium of the Univer-
color, suggesting the presence of anthocyanins, and probably other sity of Trás-os-Montes e Alto Douro with the voucher number
polyphenols, that might be related or identical to those present HVR21095.
in the berries. So elderberry wastes resultant from the elderberry
industry could be a potential low cost and alternative source of 2.3. Preparation of the elderberry berries and branches extracts
some unique natural bioactive polyphenols for other industries, like
pharmaceutical and cosmetic industries, with many applications For the exhaustive extraction of polyphenols from elder-
related to the health benefits like scavenging activity of free rad- berry berries and branches, 250 mg of freeze-dried material were
icals and anti-inflammatory properties (Murthy and Naidu, 2012; extracted with 5 mL methanol containing 1% HCl in an orbital
Nandakumar et al., 2008; Peralbo-Molina and de Castro, 2013; Ping shaker (Orbital Shaker GFL 3005 series, Hanover, Germany) for
et al., 2012; Seabra et al., 2010; Terra et al., 2007). Also polyphenols 20 min at 200 rpm. After extraction the suspension was centrifuged
may have potential uses as biobased phytosanitary products, able to (5 min at 50,000 rpm; Sigma Centrifuges 3–30 K, St. Louis, MO, USA)
control the incidence of crop diseases (Benouaret et al., 2014). The and the supernatant was removed. This process was repeated 8
use of this by-product for the extraction of valuable polyphenols times (number of exactions needed for removing all the color from
can reduce the environmental impact of some of these substances elderberry berries), and supernatants were added up and diluted to
on the cultivated fields and on the irrigation water (Kuppusamy a final volume of 50 mL with the extraction solution. For the devel-
et al., 2015; Seabra et al., 2010). Although is possible to find in the opment of a simpler and environmental friendly extraction method
literature some research on the polyphenolic content and antioxi- for elderberry branches, water and ethanol (95%) were used as sol-
dant capacity of elderberry berries and elderflowers, when we look vents. To 25 g of branches (as is basis), 1 L of solvent was added and
for information regarding to elderberry branches extracts no stud- boiled during 15 min. After cooling, the water or ethanol extracts,
ies have been done, hindering valorization. Thus, in this study we depending of the solvent used for extraction, were filtered and con-
evaluate the potential of elderberry branches, by-products of elder- centrated by rotary evaporation (Stuart RE300, Staffordshire, UK)
berries berries production, as alternative source of anthocyanins to 100 mL.
and other polyphenols. For this purpose, the polyphenolic pro-
file, total phenols, anthocyanin contents, as well the antioxidant 2.4. Determination of the total phenolic content of elderberry
activity of extracts from branches were analyzed and compared berries and branches
with those of the elderberry berries. This paper represents the first
attempt to assess the polyphenolic content and the antioxidant pro- The total phenolic content of elderberries and branches were
file of the elderberry branches from the Varosa Valley in northern determined using the Folin-Ciocalteu method according to Cheok
Portugal. et al. (2013) with some modifications. Briefly, 1 mL of properly
diluted extract was mixed with 1 mL of Folin-Ciocalteu reagent,
2 mL of sodium carbonate (7.5% w/w) and 6.5 mL of milli-Q water
2. Material and methods
and the mixture was incubated during 30 min at 70 ◦ C. After cool-
ing to room temperature, the absorbance was measured at 750 nm
2.1. Reagents
(PerkinElmer-Lambda 25, PerkinElmer, London, United Kingdom).
The total phenolic content was expressed in gallic acid equiv-
Folin–Ciocalteu’s reagent, 2,2-azino-bis(3-
alents (mg/100 g fresh weight), using a gallic acid calibration
ethylbenzothiazoline)6 sulfonic acid (ABTS),
curve.
(±)-6-hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic acid
(Trolox), methanol, sodium carbonate, gallic acid, hydrogen
2.5. Determination of the total monomeric anthocyanins of
peroxide solution, 2-deoxy-d-ribose, potassium persulfate, thio-
elderberry berries and branches
barbituric acid (TBA) and all organic solvents were purchased
from Sigma-Aldrich (Spain). Sodium nitroprusside, Sulfanil-
Total monomeric anthocyanins of elderberry berries and
amide, Naphthylethylenediamine dihydrochloride, ascorbic acid,
branches were determined using the UV–vis spectroscopy pH dif-
trichloroacetic acid were purchased from Merck (Germany).
ferential method according to Giusti and Wrolstad (2001). Two
Ethylenediamine tetraacetic acid (EDTA), Ferric(II) chloride
dilutions of elderberries and branches extracts were prepared, one
were purchased from Panreac (Spain). For HPLC analysis, ultra-
containing hydrogen chloride (pH 1.0) and the second containing
pure water was used (Milli-Q system, Millipore, Bedford, MA).
sodium acetate buffer (pH 4.5). The absorbance of both dilu-
Quercetin 3-glucoside; quercetin 3-rutinoside; isorhamnetin
tions was measured at 520 and 700 nm (PerkinElmer-Lambda 25,
3-rutinoside; isorhamnetin 3-glucoside; cryptochlorogenic
PerkinElmer, London, United Kingdom) and the total monomeric
acid; chlorogenic acid; cyanidin 3,5-diglucoside; cyanidin
anthocyanins were expressed as cyanidin-3-glucoside equivalents
3-sambubioside-5-glucoside; cyanidin 3-glucoside; cyanidin
(mg/100 g of fresh weight) using the molar extinction coefficient
3-sambubioside and quercetin were from Extrasynthese (France).
of 26,900 L cm−1 mol−1 and molecular weight of 449.2 g/mol of
Stock solutions of standard phenolic acids were prepared in
cyanidin-3-glucoside.
methanol (1 mg/mL), stored at −80 ◦ C, and used within a 1 week
period.
2.6. Determination of the antioxidant activity of elderberry
berries and branches extracts
2.2. Elderberry berries and branches samples
2.6.1. Trolox equivalent antioxidant capacity assay
The samples of elderberry berries and branches were picked in The antioxidant activity against ABTS radical was determined
quadruplicate at theoptimum fruit maturity at the end of August according to Barros et al. (2011). Briefly, the ABTS radical was
P. Silva et al. / Industrial Crops and Products 95 (2017) 227–234 229
Table 1
Percentage of humidity, total phenol content, total monomeric anthocyanins and antioxidant activity (fresh weight basis) of the branches and berries.
Humidity g/100 g Total Phenols nmg/100 g Anthocyanins mg/100 g TEACx mmol Trolox/100 g OH• scavenging % NO• scavenging mmol Trolox/100 g
Values are expressed as mean ± standard deviation (n = 4). Means within a column for each sample followed by the same letter are not significantly different (t-Student test,
p < 0.05).
x
Trolox equivalent antioxidant capacity.
230 P. Silva et al. / Industrial Crops and Products 95 (2017) 227–234
Fig. 2. Chromatograms at 280 nm, 325 nm and 525 nm of extracts from berries and branches of elderberry obtained by exhaustive methanol-1% HCl extraction. Peak
identification: 6 – quercetin 3-glucoside; 7 – quercetin 3-rutinoside; 9 – isorhamnetin 3-glucoside; 11 – cryptochlorogenic acid; −12 – chlorogenic acid; 14 – cyanidin
3,5-diglucoside; 15 – cyanidin 3-sambubioside-5-glucoside; 16 – cyanidin 3-glucoside; 17 – cyanidin 3-sambubioside; 22 – quercetin; 1, 2, 3, 4, 8, 10, 13, 18–21 and 23 –
unknown compounds.
3-sambubioside-5-glucoside was identified by comparison of its glucoside – 0.2 mg/L of extract and 1.1 mg/100 g fresh weight;
retention time in relation to the others anthocyanins described quercetin 3-rutinoside – 0.5 mg/L of extract and 2.4 mg/100 g
in the literature (Duymuş et al., 2014). For quantification of the fresh weight; isorhamnetin 3-glucoside – 1.5 mg/L of extract and
polyphenolic compounds a calibration curve was constructed in 7.5 mg/100 g fresh weight; cryptochlorogenic acid – 0.3 mg/L of
the range of 0–250 mg/mL for cyanidin 3-glucoside; cyanidin extract and 1.2 mg/100 g fresh weight; chlorogenic acid – 0.2 mg/L
3-sambubioside, and between 0 and 75 mg/L for cyanidin 3,5- of extract and 1.0 mg/100 g fresh weight; cyanidin 3,5-diglucoside
diglucoside and 0–100 mg/L for the other polyphenolic compounds – 0.05 mg/L of extract and 0.8 mg/100 g fresh weight; cyanidin
(quercetin 3-glucoside; quercetin 3-rutinoside; isorhamnetin 3- 3-glucoside – 0.2 mg/L of extract and 0.8 mg/100 g fresh weight;
rutinoside; isorhamnetin 3-glucoside; cryptochlorogenic acid; cyanidin 3-sambubioside – 0.9 mg/L of extract and 4.3 mg/100 g
chlorogenic acid; and quercetin). Cyanidin 3-sambubioside-5- fresh weight; quercetin – 1.9 mg/L of extract and 9.5 mg/100 g fresh
glucoside was quantified using the cyanidin 3-sambubioside weight. For those compounds which no standard was available cal-
calibration curve. Each calibration curve was checked for linearity ibration curves of gallic acid, chlorogenic acid and quercetin were
using the method described by (Eurachem/CITAC, 2012; Thompson used for benzoic acid derivatives, cinnamic acid derivatives and
et al., 2002), and the limits of detection and quantification were flavonoid derivatives, respectively. Recovery experiments were
determined using the residual standard deviation of the cali- performed for chlorogenic acid and the recovery obtained was
bration curve using the method described by (Eurachem/CITAC, 98.1 ± 2.7%.
2012; Thompson et al., 2002). Limits of detection: quercetin 3-
P. Silva et al. / Industrial Crops and Products 95 (2017) 227–234 231
Table 2
Amount of the polyphenolic compounds in elderberry berries and branches and concentration of extracts obtained with hot water and hot ethanol from elderberry branches
determined by HPLC.
1 2.71 ± 0.01 Unkx 275 0.094 ± 0.023a ndb 0.25 ± 0.01a 0.27 ± 0.02a
2 3.56 ± 0.01 Unk 285 0.25 ± 0.03a 0.30 ± 0.03a nd nd
3 8.22 ± 0.02 Unk 279; 288shy 0.039 ± 0.007a 1.1 ± 0.2b 0.33 ± 0.02a 0.34 ± 0.02a
4 9.16 ± 0.03 Unk 282 0.009 ± 0.002a ndb 0.18 ± 0.01a 0.21 ± 0.01b
5 43.11 ± 0.01 Quercetin-derivative 351; 258 ndz nd 1.39 ± 0.08a 1.47 ± 0.08a
6 44.21 ± 0.01 Quercetin 3-glucoside 354; 256 0.13 ± 0.02a 0.029 ± 0.006b 2.40 ± 0.15a 2.78 ± 0.17b
7 44.70 ± 0.01 Quercetin 3-rutinoside 354; 256 1.38 ± 0.19a 0.010 ± 0.001b 30.3 ± 6.7a 40.7 ± 3.5b
8 47,16 ± 0.14 Unk 281 0.006 ± 0.001a ndb nd nd
9 48.45 ± 0.02 Isorhamnetin 3-glucoside 373; 255 0.21 ± 0.03a 1.1 ± 0.1b 0.58 ± 0.44a 2.15 ± 0.58b
10 63.68 ± 0.02 Unk. 277 0.031 ± 0.001a 0.007 ± 0.002b 1.71 ± 0.03a 1.69 ± 0.02a
11 10.56 ± 0.02 Cryptochlorogenic acid 325; 297sh 0.064 ± 0.009a 0.017 ± 0.004a 0.62 ± 0.03a 0.29 ± 0.01b
12 11.61 ± 0.04 Chlorogenic acid 325; 297sh 0.006 ± 0.002a 0.012 ± 0.005b 3.77 ± 0.20a 4.56 ± 0.22b
13 39.11 ± 0.03 Unk 326; 297sh 0.21 ± 0.04a 0.34 ± 0.01b nd nd
14 20.56 ± 0.07 Cyanidin 3,5-diglucoside 512; 277 0.61 ± 0.17a 0.081 ± 0.029b 0.22 ± 0.03a 0.32 ± 0.03b
15 22.73 ± 0.13 Cyanidin 3-sambubioside-5-glucoside 513; 277 1.79 ± 0.45a 0.032 ± 0.010b 1.45 ± 0.13a 2.16 ± 0.11b
16 32.40 ± 0.19 Cyanidin 3-glucoside 513; 280 4.27 ± 0.52a 0.43 ± 0.04b 0.29 ± 0.06a 0.72 ± 0.05b
17 35.79 ± 0.20 Cyanidin 3-sambubioside 515; 280 5.59 ± 0.63a 0.12 ± 0.01b 0.97 ± 0.17a 2.33 ± 0.13b
18 18.57 ± 0.07 Unk. 294; 260 nda 0.073 ± 0.004b 0.09 ± 0.03a 0.09 ± 0.01a
19 51.43 ± 0.11 Unk 270 nda 0.012 ± 0.001b nd nd
20 36.38 ± 0.08 Unk 323; 295sh nda 2.11 ± 0.07b nd nd
21 45.34 ± 0.02 Unk. 311; 300sh nda 0.30 ± 0.02b nd nd
22 47.12 ± 0.03 Quercetin 354; 256 nda 0.021 ± 0.002b 1.39 ± 0.34a 1.87 ± 0.19b
23 47.31 ± 0.02 Unk. 324; 297sh nda 0.23 ± 0.01b nd nd
Values are expressed as mean ± standard deviation (n = 4); Means between two column for each polyphenol followed by the same letter are not significantly different
(t-Student test, p < 0.05).
w
Rt – Retention time.
v
máx – maximum wavelength.
x
Unk – unknown.
y
sh – shoulder.
z
n.d. – not detected.
232 P. Silva et al. / Industrial Crops and Products 95 (2017) 227–234
Fig. 5. Chromatograms at 280 nm, 325 nm and 525 nm of elderberry branches extracts obtained with water and ethanol. Peak identification: 6 – quercetin 3-glucoside; 7 –
quercetin 3-rutinoside; 9 – isorhamnetin 3-glucoside; 11 – cryptochlorogenic acid; 12 – chlorogenic acid; 14 – cyanidin 3,5-diglucoside; 15 – cyanidin 3-sambubioside-5-
glucoside; 16 – cyanidin 3-glucoside; 17 – cyanidin 3-sambubioside; 22 – quercetin; 1, 3, 4, 10, 12, 13 and 18 – unknown compounds.
P. Silva et al. / Industrial Crops and Products 95 (2017) 227–234 233
in the cinnamic acid derivatives (Table 2 and Fig. 4), especially the flavonols and cinnamic acids esters, presenting similar or even bet-
presence of compounds 20, 21 and 23. ter antioxidant activities when compared to berries, showing the
potential of elderberry branches as a low cost alternative source of
natural antioxidants.
3.3. Evaluation of a simpler and environmentally friendly
extraction method for elderberry branches
Acknowledgments
Methanol is usually used as good extraction solvent for
hydrophilic phenolic compounds and for the extraction of antho- The authors want to acknowledge QREN, ADI, Programa Opera-
cyanins methanol it is normally acidified (Dai and Mumper, 2010), cional do Norte and FEDER for the financial support of the Project
nevertheless the use of water or ethanol as extraction solvents are SambucusFresh n◦ 23109 and to the financial support provided to
more safe (Dai and Mumper, 2010; Shi et al., 2005) and environ- the Research Unit in Vila Real (PEst-OE/QUI/UI0616/2014) by FCT
mentally friendly (Corrales et al., 2009). Especially ethanol due and COMPETE.
to its physicochemical characteristics (low boiling point) make
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