Antioxidant Capacities of Some Food Plants Wildly Grown in Ayvalik of Turkey

Food Sci. Technol. Res., 15 (1), 59–64, 2009

Antioxidant Capacities of Some Food Plants Wildly Grown in Ayvalik of Turkey

Kerim alpinar1, Mustafa ÖzYüreK

2, Ufuk KolaK1, Kubilay güçlü

2, Çiğdem aras3, Mehmet altun

2, Saliha Esin çeliK

2, Kadriye Işıl berKer2, Burcu beKtaşoğlu

2, and Reşat apaK2*

1 Department of General Chemistry, Faculty of Pharmacy, Istanbul University 34116 Beyazıt, Istanbul, Turkey2 Department of Chemistry, Faculty of Engineering, Istanbul University 34320 Avcılar, Istanbul, Turkey3 Pharmacy Aras, Ayvalik, Balıkesir, Turkey

Received April 17, 2008; Accepted October 27, 2008

This study aims to investigate the total antioxidant capacity (TAC) as trolox equivalent (mmol g-1) of nineteen edible wild plants traditionally used in Ayvalik using four different assays, CUPRAC, ABTS, FRAP and Folin. The order of ten plants exhibiting the higher capacities could be listed as: Daucus carota (1st wrt CUPRAC, ABTS, and FRAP), Sonchus oleraceus (2nd wrt CUPRAC, ABTS, and FRAP), Sonchus

asper (3rd), Rumex pulcher (4th wrt CUPRAC, ABTS, and Folin), Cichorium intybus (5th wrt CUPRAC, ABTS, and Folin), Papaver rhoeas (7th wrt CUPRAC, ABTS, and FRAP), Foeniculum vulgare (8th wrt CUPRAC and FRAP), Urtica pilulifera (6th wrt CUPRAC, 8th wrt Folin), Rumex acetosella (7th wrt Folin, 9th wrt CUPRAC and FRAP), and Nasturtium officinale (11th wrt CUPRAC and Folin). The three edible wild plants (Daucus carota, Sonchus asper subsp. glaucescens and Sonchus oleraceus) with CUPRAC anti-oxidant capacities of 0.37±0.05, 0.31±0.03, and 0.34±0.05 mmol trolox g-1, respectively, may be considered as a potential source of natural antioxidants to be incorporated in current diets to protect human health. CUPRAC method proved to be most effective among electron-transfer based TAC assays since it respond-ed to a wide variety of hydrophilic and lipophilic antioxidants.

Keywords: ayvalik food plants, antioxidant capacity, CUPRAC (cupric reducing antioxidant capacity) assay

*To whom correspondence should be addressed.

Email: [email protected]

IntroductionThe quality of food has increased by using antioxidants

which have prevented or delayed their oxidative deteriora-

tion during processing and storage (Cosio et al., 2006). Wild

plants, vegetables and fruits have attracted much attention

as sources of natural antioxidants. Many of the wild plants,

vegetables and fruits contain antioxidants such as vitamins

(β-carotene, vitamins C and E), and polyphenols (flavonoids,

tannins, catechins) (Wong et al., 2006). Epidemiological

studies have shown that a diet rich in vegetables and fruits

can reduce the incidence of cardiovascular diseases and of

certain cancers (Ames, 1983; Block et al., 1992).

Ayvalik is located in the northwestern part of Anatolia

(Turkey) where the use of wild edible plants is a practice that

has developed over generations and is part of the local tradi-

tional knowledge system. The Maritime climate dominates

in Ayvalik where the summers are hot and dry while the

winters tepid and rainy (Temucin, 1993). The sub-humid cli-

mate around Ayvalik enables the widest distribution of plant

species. The inhabitants in Ayvalik consume the aerial parts

of various food plants listed in Table 1 with botanic, English,

and local names. Esiyok et al. (2004) have reported a brief

overview of important herbs in the Turkish flora, including

fennel, mallow, chicory, nettle, wild radish, and wild mus-

tard, as important food plants for promoting human health

and preventing cancer.

Total antioxidant capacity may better reflect the health

beneficial quality of foods than individual measurements due

to the possible cooperative action of antioxidants (Ghiselli

et al., 2000). The aim of this study is to investigate the total

antioxidant capacity as trolox equivalent (mmol g-1) of nine-

teen wild edible plants traditionally used in Ayvalik as food

plant and dietary supplement. In this study, the antioxidant

capacity of the methanol extracts of A. nodiflorum, P. rhoeas

var. rhoeas, S. dichotoma subsp. dichotoma, S. asper subsp

glaucescens, N. officinale, S. arvensis, U. pilulifera, R. aceto-

sella, T. communis subsp cretica, S. hispanicus, O. hispidus,

K. alpinar et al.

Table 1. The total antioxidant capacities in trolox (TR) equivalents of nineteen edible wild plants grown in Ayvalik as assayed by CUPRAC, ABTS/persulfate, FRAP, and Folin methods.

Edible plantsgrown in Ayvalik

Englishand/or local

names

TEACCUPRAC(mmol TR g–1)

TEACABTS(mmol TR g–1)

TEACFRAP(mmol TR g–1)

TEACFolin(mmol TR g–1)

1 Malva sylvestris L.–ISTE 71775

Blue mallow,ebegümeci

0.07±0.001 0.05±0.002 0.02±0.001 0.13±0.011

2 Raphanusraphanistrum L.–ISTE 71277

Wild radish,turp otu

0.06±0.011 0.03±0.004 0.02±0.010 0.11±0.008

3 Foeniculum vulgareMiller –ISTE 68224

Fennel, rezene 0.12±0.026 0.16±0.032 0.06±0.006 0.22±0.047

4 Apium nodiflorum(L.) Lag.–ISTE30637

Fool’sWatercress,

kereviz

0.11±0.013 0.13±0.029 0.04±0.003 0.18±0.020

5 Papaver rhoeas L.var. Rhoeas–ISTE71809

Corn poppy,gelincik

0.13±0.008 0.15±0.031 0.07±0.028 0.25±0.016

6 Silene dichotomaEhrh. subsp.dichotoma –ISTE74148

Forkedcatchfly,

yapışkan otu

0.05±0.002 0.05±0.003 0.02±0.001 0.14±0.049

7 Cichorium intybusL.–ISTE 73569

Chicory,hindiba

0.21±0.009 0.17±0.017 0.09±0.010 0.38±0.016

8 Sonchus asper (L.)Mill. subsp.glaucescens(Jordan) Ball –ISTE71615

Spinysowthistle,

eşek marulu

0.31±0.026 0.20±0.020 0.10±0.004 0.42±0.024

9 Nasturtiumofficinale R.Br. –ISTE 46162

Watercress,su teresi

0.11±0.024 0.10±0.004 0.08±0.001 0.18±0.024

10 Sinapsis arvensis L.–ISTE 73606

wild mustard,yabani hardal

0.04±0.006 0.04±0.006 0.02±0.002 0.12±0.012

11 Urtica pilulifera L.–ISTE 71611

Roman nettle,kara ısırgan

0.16±0.007 0.09±0.012 0.05±0.006 0.23±0.014

12 Rumex acetosella L.–ISTE 68184a

sheep sorrel,kuzu kulağı

0.12±0.030 0.09±0.009 0.06±0.026 0.25±0.116

13 Tamus communis L.subsp. cretica (L.)Kit Tan –ISTE74109

Black bryony,tilki üzümü

0.05±0.020 0.06±0.003 0.01±0.001 0.15±0.053

14 Scolymushispanicus L. –ISTE 74224

Golden thistle,sarı diken

0.06±0.013 0.03±0.010 0.02±0.005 0.10±0.001

15 Opopanax hispidus(Friv.) Griseb. –ISTE 46146

Sarı ot 0.08±0.010 0.08±0.032 0.03±0.002 0.20±0.040

16 Rumex pulcher L.–ISTE 73530

Fiddle dock 0.25±0.044 0.18±0.015 0.08±0.001 0.40±0.018

17 Sonchus oleraceusL. –ISTE 71345

sowthistle,helvacık

0.34±0.054 0.25±0.009 0.10±0.005 0.59±0.018

18 Daucus carota L.–ISTE 73552

wild carrot,yabani havuç

0.37±0.046 0.26±0.015 0.13±0.007 0.52±0.051

19 Salicorniaeuropaea L.–ISTE 73061

jointedglasswort,

deniz börülcesi

0.07±0.009 0.11±0.023 0.03±0.002 0.14±0.014

60

and R. pulcher is reported for the first time. In addition, the

antioxidant capacities of M. sylvestris, R. raphanistrum, C.

intybus, S. oleraceus, D. carota, and S. europaea were inves-

tigated for the first time using CUPRAC (Apak et al., 2004;

2005; 2006; 2008), ABTS/persulfate (Re et al., 1999), FRAP

(Benzie and Strain, 1996) and Folin (Singleton et al., 1999)

assays. Additionally, three antioxidant assay methods with

the exception of Folin were used to determine the antioxidant

capacity of F. vulgare for the first time.

Materials and MethodsMaterials Neocuproine and Folin-Ciocalteou reagent

were purchased from Sigma Chemical Co. (Sigma-Aldrich

GmbH, Steinheim, Germany). Trolox was obtained from

Aldrich Chemicals Co. (Sigma-Aldrich GmbH, Steinheim,

Germany). Ammonium acetate, copper (II) chloride, po-

tassium persulfate, hydrochloric acid, sodium hydroxide,

copper (II) sulfate, sodium carbonate, sodium potassium

tartarate, glacial acetic acid, sodium acetate trihydrate, fer-

ric chloride hexahydrate, ethanol (96%) and methanol were

purchased from Merck (Darmstadt, Germany), 2,2’-azinobis

(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt

(ABTS) and 2,4,2-tri(2-pyridyl)-s-triazine (TPTZ) from Flu-

ka Chemical Co. (Buchs, Switzerland). All other chemicals

and solvents were analytical grade.

Copper(II) chloride (1.0×10-2 M) and ammonium acetate

buffer (1.0 M, pH=7.0) were prepared in water while neo-

cuproine (Nc : 7.5×10-3 M) and trolox (1.0×10-3 M) in 96%

ethanol. To a 7.0 mM aqueous solution of ABTS radical re-

agent, K2S2O8 was added to attain a final persulfate concen-

tration of 2.45 mM. The resulting ABTS radical cation solu-

tion was left to mature at room temperature in the dark for

12-16 h, and then used for TEAC assays. The solutions used

in the Folin assay of polyphenolics were prepared as follows:

Lowry A: 2% aqueous Na2CO3 in 0.1 M NaOH; Lowry B:

0.5% CuSO4 aqueous solution in 1% NaKC4H4O6 solution;

Lowry C: prepared freshly as mixture (50 mL Lowry A +

1 mL Lowry B); Folin-Ciocalteau reagent was diluted with

H2O at a volume ratio of 1:3 prior to use. All percentages are

given as (w/v), and distilled and deaerated (N2-bubbled) wa-

ter was used throughout. The FRAP solutions were freshly

prepared as follows: FeCl3 solution (2.0×10-2 M) was pre-

pared in water containing 0.02 M HCl, TPTZ (1.0×10-2 M) in

96% EtOH, and acetic acid buffer (0.3 M, pH=3.6) in water.

The acetic acid buffer, TPTZ solution, and FeCl3 solution

were mixed in this order at a volume ratio of 10:1:1.

Plant material Plant materials were obtained from Ay-

valik local market by Mrs. Çiğdem Aras (Pharm.) in April

2006 and identified by Dr. Kerim Alpınar from Istanbul

University. Voucher specimens were kept in the Herbarium

of the Faculty of Pharmacy, Istanbul University (ISTE). The

scientific and vernacular names of the specimens including

their families and numbers are presented in Table 1.

Instruments All spectrophotometric measurements were

made with a pair of matched quartz cuvettes using a Varian

CARY 1E UV-Vis spectrophotometer. Ultra-Turrax CAT

X620 apparatus was used for extraction. An Adams Dynac

centrifuge apparatus was used for separation of the clear

fractions of plant extracts.

Solvent extraction of plant materials Aerial parts of the

plant materials were dried and powdered by using Waring

blender. The humidity of plant materials were estimated by

drying in an oven at 105℃ for 2 h. The dry plant specimens

were crushed in a mill, and 2-g samples were taken for each

plant species. These samples were soaked in 80% MeOH

overnight, and homogenized in an Ultra-Turrax apparatus

by gradually increasing the number of cycles per unit time.

The obtained extracts were centrifuged for 10 min, and sub-

sequently filtered through a filter paper into 100-mL flasks.

The same procedure was repeated 3 times with 25 mL por-

tions of 80% MeOH on the remaining part of the plants. All

filtered extracts were combined, and diluted to 100 mL using

the same solvent (Güçlü et al., 2006). The obtained extracts

were analyzed for their antioxidant capacities on the next

day after preserving the N2 –bubbled and stoppered extracts

in a refrigerator at + 4℃. The antioxidant capacities of plant

samples were reported based on dry matter content.

Total antioxidant capacity assays

CUPRAC assay To a test tube, the following solu-

tions were added: 1 mL CuCl2, 1 mL neocuproine, and 1

mL NH4Ac buffer, and mixed; 0.5 mL of dilute plant extract

(previously diluted with MeOH at a volume ratio of 1:10)

followed by 0.6 mL of water were added (total volume = 4.1

mL), and mixed. Absorbance against a reagent blank was

measured at 450 nm after 30 min (the tested plant extracts

were checked to reach steady state absorbance within this pe-

riod). The trolox equivalent molar concentration of the plant

extract sample in final solution may be found by dividing the

observed absorbance to the molar absorptivity (ε) for trolox

(optical cuvette thickness = 1 cm).

ABTS/Persulfate assay The matured ABTS radical so-

lution of blue-green colour was diluted with ethanol at a ratio

of 1:10. To 1 mL of the 1: 10 diluted radical cation solution,

4 mL of ethanol were added, and the absorbance at 734 nm

was read at the end of the sixth minute. The procedure was

repeated for the unknown plant extract by adding 1 mL of

the radical cation solution to x mL (x = 0.2 or 1 mL) of dilute

plant extract (previously diluted with MeOH at a volume

ratio of 1:10) and (4-x) mL of ethanol, and recording the ab-

sorbance at the end of the sixth minute. The absorbance dif-

Antioxidant Capacities of Food Plants in Ayvalik 61

ference (∆A) was correlated to trolox equivalent antioxidant

concentration with the aid of a linear calibration curve.

FRAP assay of total antioxidant capacity To 3 mL of

the FRAP reagent was added 0.3 mL H2O. Then 50 or 100

µL aliquots of the plant extracts were taken, and 96% EtOH

was added to make the final volume 3.4 mL. The absorbance

at 595 nm (A595) was read against a reagent blank at the end

of 6 min, and correlated to TEAC of the plant.

Folin total phenolic content To 0.5 mL of the dilute

plant extract (previously diluted with MeOH at a volume

ratio of 1:10) was added 1.5 mL H2O. An aliquot of 2.5 mL

of Lowry C solution was added, and the mixture was let to

stand for 10 min. At the end of this period, 0.25 mL of Folin

reagent was added, and 30 more min was allowed for stabi-

lization of the blue colour formed. The absorbance against a

reagent blank was measured at 750 nm.

Results and DiscussionThe extracting solvent, optimally selected as 80% (v/v)

methanol, gave satisfactory results (Zielinski and Kozlowska,

2000), better than pure water or less MeOH-containing

solvent extractions, in terms of total phenolic content and

antioxidant activity of the extract. Aqueous MeOH (80%) ap-

pears to be the best solvent for many varieties of phenolics,

flavonoids, and other semi-polar antioxidants (Siddhuraju

and Becker, 2003).

Table 1 shows the antioxidant capacities of the plants

with respect to the four assays tested. Generally the assay

results correlated well among each other, because all were

basically electron transfer (ET) - based assays (Huang et al.,

2005) having a similar mechanism. For example, the CU-

PRAC results tabulated in Table 1 correlated linearly with

those of other assays, given by the equations:

TEACCUPRAC = 1.35 TEACABTS – 0.0158 ... (r = 0.926);

TEACCUPRAC = 2.74 TEACFRAP – 0.0057 ... (r = 0.923);

TEACFolin = 1.36 TEACCUPRAC + 0.0545 ... (r = 0.972).

CUPRAC results correlated significantly with those of

other assays at 95% confidence level, tested with the t-test

using the equation: tcalcd. = |r| ( )( )2

n 21 r−

−, where r is the correla-

tion coefficient, n is the number of measurements, and

(n-2) is the degrees of freedom (Miller and Miller, 1993).

Since the calculated value of t for each binary correlation

was greater than the tabulated value of t using a two-tailed

t-test, a significant correlation did exist between the results

of the CUPRAC and other assays. The highest correlation

of CUPRAC was obtained with Folin. Although Cu(II)– and

Fe(III)– reducing antioxidant assays seemingly had close re-

dox potentials (Apak et al., 2004; 2005; Berker et al., 2007),

CUPRAC is capable of measuring a greater variety of anti-

oxidant compounds –regardless of their hydrophilicity– than

FRAP. The CUPRAC-Folin correlation was better than those

of most other antioxidant tests with Folin, as also confirmed

by Park et al. (2008) for ethylene-treated kiwifruits. The

highest results of antioxidant capacity were obtained with the

Folin test, because the molybdato-phospho-tungstate hetero-

poly acid reagent of this test had the highest redox potential

in alkaline medium where most phenolic compounds are de-

protonated and open to oxidative attack (Apak et al., 2007).

The second highest results were obtained with CUPRAC

due to the completion of the colour reaction within the speci-

fied time period, as reported in other papers of the authors,

whereas the FRAP method does not respond efficiently to

thiol (–SH) type antioxidant compounds (Apak et al., 2004;

Berker et al., 2007; Gorinstein et al., 2006).

The TEAC order for hydroxycinnamic acids of CUPRAC

is just the reverse of that of ABTS/TEAC (i.e., caffeic and

chlorogenic acids have higher TEAC: trolox equivalent

antioxidant capacity values than ferulic or p-coumaric acids

in the CUPRAC method) (Apak et al., 2004; 2007). This

may be the reason of the significant differences between the

CUPRAC and ABTS results of fennel (Foeniculum vulgare

Miller) and Roman nettle (Urtica pilulifera L.) (plants 3

& 11, respectively, in Table 1) that are known to contain

hydroxycinnamic acids, e.g., chlorogenic, neochlorogenic,

dicaffeoylquinic and rosmarinic acids in fennel (Parejo et

al., 2004). Likewise, in spite of the fact that the polyphenolic

contents of Sonchus species may differ widely depending on

geography and climate (Schaffer et al., 2005), Sonchus spe-

cies (plants 8 & 17 in Table 1) had the highest (2nd and 3rd)

capacities among the plants tested, much higher than those

found by ABTS and FRAP assays, probably because their

carotenoid contents (Guil-Guerrero et al., 1998) could not be

completely assayed by ABTS and FRAP methods, whereas

CUPRAC is capable to assay carotenoids in 80% MeOH so-

lution (Apak et al., 2007). Additionally, it is noteworthy that

the FRAP results for the mentioned plant extracts as well as

for a majority of others were extremely low possibly due to

incomplete oxidation by the FRAP reagent.

El and Karakaya (2004) studied nine species of greens

from different families native to the Aegean region of Tur-

key; the order they found for DPPH• radical scavenging

activity was: wild carrot > fennel > chicory > sowthistle

> jointed glasswort > corn poppy > wild radish. It can be

seen that the leading DPPH• scavenging species like Daucus

carota, Cichorium intybus, and Sonchus oleraceus (El and

Karakaya, 2004) are also the ones with high antioxidant ca-

pacity, as measured in this work. Antioxidant and anti-radical

activities were reported in the literature for certain plants

K. alpinar et al.62

without mentioning active constituents, e.g., xanthine oxi-

dase inhibiting activity for aerial parts of chicory and DPPH•

scavenging activity for aerial parts of Apium nodiflorum

(Pieroni et al., 2002), polyphenolic antioxidant capacity for

aerial parts of Sonchus oleraceus L. and leaves of Cichorium

intybus L. (Schaffer et al., 2005). Daucus carota L. species

collected at random from Jordan’s flora showed antioxidant

capacities -using the ABTS/TEAC method- of 75.8 and 49.0

µmol trolox equivalent g-1 dry weight in aqueous and metha-

nolic extracts, respectively (Alali et al., 2007).

ConclusionsTotal antioxidant capacities of nineteen edible wild plants

grown in Ayvalik (Turkey) were assayed by CUPRAC,

ABTS, FRAP and Folin methods. Since it has been accepted

nowadays that both hydrogen atom transfer (HAT) - and

electron transfer (ET) - based assays are needed to give a re-

liable estimate of the antioxidant capacity of foods, a mixed

mechanism (i.e., HAT- and ET- based) assay such as ABTS

was included among the ET- based assays preferred in this

work. For most plants characteristic to the region, reporting

of antioxidant capacity with classical assays is accomplished

for the first time. There was good linear correlations among

results obtained with different assays. The order of reported

CUPRAC antioxidant capacities-as trolox equivalents- was

Daucus carota > Sonchus oleraceus > Sonchus asper >

Rumex pulcher > Cichorium intybus > Urtica pilulifera >

Papaver rhoeas > Foeniculum vulgare > Rumex acetosella >

Nasturtium officinale. The three edible wild plants (Daucus

carota, Sonchus asper subsp. glaucescens and Sonchus ol-

eraceus) may be considered as a potential source of natural

antioxidants, and can be especially recommended to be in-

corporated in current diets to protect human health and serve

general wellness. The CUPRAC antioxidant capacity assay

is simultaneously cost-effective, rapid, stable, selective, and

suitable for a variety of antioxidants regardless of chemical

type or hydrophilicity. CUPRAC may enable easy identifica-

tion and classification of a variety of edible plants with re-

spect to their antioxidant properties.

Acknowledgments The authors would like to express their grati-

tude to the State Planning Organization of Turkey for the Advanced

Research Project of Istanbul University (2005K120430). The au-

thors also extend their gratitude to TUBITAK (Turkish Scientific

and Technical Research Council) for the Research Projects 105T402

and 106T514.

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