Mal J Nutr 8(2): 179-189, 2002

Antioxidant Activity of Commonly Consumed Vegetables in Yemen

Mohammed Ali Al-Mamary

Department of Organic Chemistry, Faculty of Pharmacy, Sana’a University

Sana’a, P.O.Box 13697, Yemen. E-mail : almamarym@hotmail.com

ABSTRACT

Of late, more attention has been paid to the role of natural antioxidants, especially phenolic
compounds, which may act both by reducing the content of toxic compounds in foods and by
supplying the human body with exogenous antioxidants. The total phenolic contents and the total
antioxidant activities (% AA) of 17 commonly consumed vegetables in Yemen were determined.
Total phenolics was measured colorimetrically using the Folin-Ciocalteu reagent with D-catechin
as the standard. The antioxidant activity (%AA) of vegetables using their juices at different
levels (50µl, 100µl, 200µl) was assayed in vitro by the inhibition of liver homogenate oxidation
mediated by FeSO4 / ascorbate system. The % AA was measured by the TBAR method. The
results showed that for all vegetable juices, increased antioxidant activity or decreased
prooxidant activity increased with volume of juice. With the addition of 50µl from each sample,
most vegetable juices showed antioxidant activity and it appears that coriander had exceptionally
high antioxidant activity (60%). However, garlic, yellow onion, parsley, red onion and Cissus
rotundifolia showed considerably high antioxidant activities (54–41 %). Other vegetables with
low antioxidant activities (27 to 3 %) showed an order of increase in %AA as follows: tomato >
spinach > horseradish-leaves > carrot > cabbage > chilli > leek > horseradish-roots. At the same,
time some vegetable juices such as that of green pepper, cucumber and lettuce showed initial
prooxidant activities (–11 to –40 %). The complete inhibition of oxidation was noticed when the
highest level of juices (200µl) was used in the cases of coriander, onions, garlic and parsley. The
correlation between total phenolics and the antioxidant activities of vegetables with different
levels of juices (50µl, 100µl and 200µl) showed positive but not significant correlations (R =
0.41 - 0.55). Some vegetables such as carrots and tomatoes show the highest relative antioxidant
efficiencies despite the small content of total phenolics compared to other vegetables tested in
this study.

INTRODUCTION

Fatty acyl side chains peroxidation in biological membranes by reactive oxygen species and
transition metal ions in a free radical chain reaction can be deleterious for membrane
permeability as it can produce toxic compounds in humans, such as malonaldehyde (MA) and
acetaldehyde, which in turn produce abnormal adducts with biological substances, including
DNA and RNA (Feinman, 1988; Esterbauer, Schaur & Zollner, 1991). Furthermore, a strong
relationship between atherosclerosis and acetaldehyde formed from lipid peroxidation has been
reported (Glavind et al., 1952).
 Mohammed Ali Al-Mamary

Most living organisms possess enzymatic and nonenzymatic defence systems against excess
production of reactive oxygen species. However, different external factors such as smoke, diet,
alcohol and some drugs and aging could decrease the capability of such protective systems
resulting in disturbances of the redox equilibrium that is established in healthy conditions.
Therefore, antioxidants that scavenge reactive oxygen species may be of great value in
preventing the onset and/or the propagation of oxidative diseases (Willet, 1994). Antioxidants
are also compounds that inhibit or delay the oxidation of other molecules by inhibiting the
initiation or propagation of oxidizing chain reactions (REF.). Of late, more attention has been
paid to the role of natural antioxidants mainly phenolic compounds, which may have more
antioxidant activity than vitamins C, E, β-carotene (Vinson et al., 1995a), and lycopene (a
carotenoid without provitamin A) (Arab and Steck, 2000; Matos et al., 2001; Giovannucci et al.,
2002). The antioxidative effects of natural phenolic compounds in pure forms or in their extracts
from different plant sources such as vegetables, fruits and medicinal plants were studied in vitro
using different model systems of oxidation (Heinonen, Meyer & Frankel, 1998; Velioglu et al.,
1998; Gazzani et al., 1998a; Gazzani et al., 1998b, Vinson et al., 1998; Meyer et al., 1998;
Pietta, Simonetti & Mauri, 1998; Yen & Hsieh, 1998) led to speculation about the potential
benefits of ingestion of plant phenolics. Therefore, antioxidants, which can neutralize free
radicals, may be of central importance in the prevention of carcinogenicity, cardiovascular and
neurodegenerative changes associated with aging (Halliwell, 1994; Yu, 1994). Epidemiological
studies show that the consumption of vegetables and fruits can protect humans against oxidative
damage by inhibiting or quenching free radicals and reactive oxygen species (Ames, Shigena &
Hagen, 1993).

Increased generation of reactive oxygen species and oxidative stress are hypothesized to play an
important role in the pathology of diabetes (Wolff, 1993). Oxidized lipoproteins play a major
role in the development of atherosclerosis and in diabetic vascular complications (Baynes, 1991).
The alterations of low density lipoprotein (LDL) mediated by elevated glucose levels may
contribute to the atherogenesis and vascular disease in diabetes. Furthermore, raised levels of
low density lipoprotein-cholesterole and reduced high density lipoprotein-cholesterole / low
density lipoprotein-cholesterole (HDL-C/LDL-C) ratio are often observed in diabetes and are
risk factors for atherosclerosis (Beteridge, 1989). Humans are constantly exposed to reactive
oxygen species produced by natural phenomena such as ultraviolet light or by anthropogenic
activities (for example, automobile exhaust). Therefore, supplementing antioxidants to scavenge
undesirable reactive oxygen species is very important to prevent in vivo oxidative damage.

The aim of the present work is to evaluate in vitro the antioxidant activities of commonly
consumed fresh vegetables in Yemen in relation to their total phenolic contents.

MATERIALS AND METHODS

Sample collection

All vegetables used in this experiment were grown in Yemen, freshly obtained from a local
market and were in good condition. The vegetable samples were parsley, green pepper, yellow
 Antioxidant Activity of Commonly Consumed Vegetables in Yemen

onion, red onion, chilli, leek, carrot, cucumber, tomato, horseradish, spinach, garlic, coriander,
lettuce, Cissus rotundifolia (halas is the local name) and cabbage.

Preparation of vegetable samples

All vegetables were washed with tap-water followed by distilled water, but onion and garlic were
first cleaned and peeled before washing. 300 g of each vegetable were minced, mixed well and a
known amount (50 to 60 g) from each sample was transferred to a double-folded cheesecloth
placed on a funnel. The juice was filtered through the cheesecloth by using fingers to press the
sample if necessary. The volume obtained from each sample was measured (Table 1) and divided
into two tubes for studying the antioxidant activity and to determine the total phenolic contents.

The preparation of liver homogenate

Adult male guinea pigs were obtained from the Experimental Farm of the Faculty of Agriculture,
Sana’a University. The animals were maintained on a formulated diet to fulfil their nutritional
requirements. Feed and water were provided ad libitum. The animals were fasted overnight and
the day after were killed and the liver from each animal was collected and dissected and a 20 %
homogenate was prepared in ice cold phosphate buffer, pH 7.4 (Anuradha & Pavikumar, 1998)
and centrifuged at 20000 g (Sorval RC-5B Refrigerated Superspeed Centrifuge) for 15 min in a
refrigerated centrifuge to remove the cell debris. The supernatant was used for the in vitro
studies.

Antioxidant activity toward lipid peroxidation in liver homogenate

The effect of different types of vegetable juices on FeSO4/ascorbate-induced peroxidation in

liver was assessed using an incubation mixture, containing 0.4 ml of tissue homogenate, 4.0 ml
of the oxidizing solution (50µmol/L FeSO4; 1mmol/L KH2PO4; 0.2 mmol/L ascorbic acid in
0.15 M Tris-HCl buffer, pH 7.4), and different volumes of vegetable juices (50µl; 100µl; 200µl).
Incubation was carried out in a water bath at 37°C + for 20 min. The tubes were shaken every 5
min. The reactions were stopped by the addition of 1.0 ml of 10% trichloroacetic acid (TCA)
after the incubation period. The tubes were shaken well and 1.5 ml of thiobarbituric acid (TBA)
(1% in 0.05 N NaOH) reagent was added and heated at 80°C + for 30 min. The tubes were
centrifuged at 5000 g for 10 min and the colours developed in the supernatant were read at 532
nm (Milton Roy Spectronic 1001 plus) (TBARS1). As the control, the homogenate was
peroxidized by FeSO4 / ascorbate without the antioxidants (TBARS2). The reactions without
FeSO4 / ascorbate were carried out for each of the test substance as the blank (TBARS3 is the
blank for test and TBARS4 is the blank for control). The antioxidant potential of the sample was
calculated by using the following equation:

Antioxidant activity (%)

= (1- (TBARS1 - TBARS3) /
(TBARS2 - TBARS4) X 100

All tests were done in triplicate and the results averaged.

 Mohammed Ali Al-Mamary

Table 1. The total phenolics of tested vegetables

No Vegetable Name ml/g TPh (mg / 100g FW)

Common Latin FW Dw

1 Corainder Coriandum sativum 0.69 122.01±1.05 701.21±6.07

2 Garlic Allium sativum 0.42 95.75±1.22 292.81±3.74
3 Parsley Petroselinum sativum 0.54 193.46±4.22 1186.89±25.88
4 Onion (Yellow) Allium sphaeroephalum cepa 0.71 64.86±1.46 505.59±16.60
5 Onion (Red) Allium sphaeroephalum cepa 0.69 64.18±1.58 513.44±12.60
6 Halas Cissus rotundifolia 0.59 61.97±1.53
7 Tomato Lycopersicum esculantum 0.89 28.85±0.93 506.20±16.34
8 Spinach Spinocia oleracea 0.75 106.31±1.46 1417.47±19.47
9 Horseradish leaves Raphanus sativum 0.71 96.08±0.43 1117.17±4.98
10 Carrot Daucus carota 0.56 22.33±1.22 194.17±10.65
11 Cabbage (white) Brassica oleracea 0.49 26.24±0.69 354.55±9.33
12 Chilli Caspicum sp. 0.56 116.03±2.47 1084.36±14.48
13 Leek Allium schoenoprasum 0.73 90.71±6.91 621.30±47.32
14 Horseradish roots Raphanus sativum 0.59 38.25±2.54 597.60±39.63
15 Lettuce Lactuca sativa 0.69 56.45±0.76 1085.58±14.58
16 Cucumber cucumis sativum 0.87 12.38±0.99 371.66±60.83
17 Pepper (Green) Capsicum annum 0.71 73.19±1.38 938.33±17.70

TPh = Total Phenolics, FW= Fresh weight, DW= Dry weight

Determination of the total phenolic contents

The concentration of total phenolic contents in vegetable juices was determined by Folin-
Ciocalteu procedure (Sigleton & Rossi, 1965) and expressed as mg/100 g of fresh weight
vegetable as catechin equivalent (CE).

Statistical analysis

Differences in antioxidant activities and correlations between phenolic contents in vegetables

and their antioxidant activity were tested by one-way analysis of variance and regression
analysis, respectively using a simple statistical package. Significane level was P<0.05 unless
otherwise indicated.

RESULTS

The percentage of antioxidant activities calculated after the addition of 50µl, 100µl, and 200µl
from each vegetable juice to the reaction mixture incubated at 37°C for 20 min was measured by
the thiobarbituric acid reagent substances (TBARS) method as a % inhibition of liver
homogenate oxidation (Table 2). This study shows that all vegetable juices either exhibited
increased antioxidant activity or decreased prooxidant activity with increasing juice
concentration. Therefore, their behavior differed according to the type of vegetable and volume
of juice added to the system.
 Antioxidant Activity of Commonly Consumed Vegetables in Yemen

The addition of 50 µl from each sample to the reaction mixture showed that most of the
vegetable juices have varying levels of antioxidant activities with coriander having the highest
antioxidant activity (60%). Garlic, yellow onion, parsley, red onion, and C. rotundifolia. also
showed moderate antioxidant activities (54 - 41%). Other vegetables, which showed low
antioxidant activities in the range of between 26.58 and 2.81% showed the following order of
increase in antioxidant activities: tomato > spinach > horseradish-leaves > carrot > cabbage >
chilli > leek > horseradish-roots. At the same time some vegetable juices such as green pepper,
cucumber, and lettuce showed initial prooxidant activities and were in the range of –10.50 to –
39.99 %. When 100 µl of vegetable juices was used, almost none of the vegetable juices led to
complete inhibition of liver homogenate oxidation as expected especially in the case of coriander
and garlic. However, the addition of 200 µl of vegetable juice of only coriander, garlic, onions
and parsley into the mixture showed almost complete inhibition of liver homogenate oxidation
(Table 2).

The present results do not show a clear dose-relationship between the total phenolic contents and
the antioxidant activities. Parsley contains the highest total phenolics (193.27 mg /100 g wet
weight), but at the level of 50 µl of juice, its antioxidant activity (48.82 %) was lower than that of
coriander (60.11 %) with total phenolic contents of 121.41 mg / 100 g wet weight. This was
seen more clearly when we compared the total phenolics of yellow onion (65.13 mg/100 wet
weight) and red onion (63.81 mg/100 g wet weight) with the total phenolics of green pepper
(73.19 mg/100g wet weight), which was significantly higher than those of onions. Green pepper
showed prooxidant activity even with an increase in the volume of its juice (50µl - 200µl). In
general, the absence of linear correlation between total phenolics and antioxidant activities was
also noticed when similar in vitro studies were carried out using different vegetables, fruits and
medicinal plants (Gazzani et al., 1998a; Gazzani et al., 1998b; Velioglu et al., 1998). To further
investigate the relative antioxidant efficiency of total phenolics in each vegetable, the
antioxidants of the vegetables in this study were related to that of parsley as it contained (Table
3) the highest total phenolic contents (193 mg/100 FW), and having total antioxidant activity of
49.16, 81.98 and 95.12 % with diferent levels of juice (50µl, 100µl and 200µl respectively).
Thus, the expected antioxidant activities of total phenolics in vegetables were calculated
according to the following equations:

EAA (%) = TPHt X AAr

TPHr

and the EAA (%) = Aat (%)

EAA (%)

where, EAA = the expected antioxidant activity of tested vegetable at any level of juice obtained
theoretically, TPHt = the total phenolics of tested vegetable (mg /100g FW), TPHr = the total
phenolics of parsley (mg/100g FW), AAr = the antioxidant activity of parsley at the same tested
level of juice, AAt = the antioxidant activity of tested vegetable obtained from the experiment at
any level of juice, and RAE = the relative antioxidant efficiency of tested vegetable.
 Mohammed Ali Al-Mamary

Table 2. Relationship between total phenolic contents (mg / 100g FW) and antioxidant activities
of vegetables (% AA)

No. Name of vegetable Antioxidant activity (% AA) T Ph. (mg/100g FW)

50µl 100µl 200µl

1 Coriander 59.81±2.13 a 93.55±1.76 a 98.65±0.04 a 122.01±1.05 b

2 Garlic 53.25±0.44 b 84.60±1.03 b 93.68±2.11 c 95.75±1.22 e
3 Parsley 49.16±2.19 c 81.98±1.25 c 95.12±2.93 bc 193.46±4.22 a
4 Yellow onion 49.42±0.61 c 82.67±0.40 c 95.30±0.83 bc 64.86±1.46 g
5 Red onion 46.20±1.96 d 85.65±0.84 b 96.46±0.30 b 64.18±1.58 g
6 C. Rotundifolia 41.26±3.96 d 69.95±0.13 d 85.92±1.64 d 61.97±1.53 g
7 Tomato 26.36±0.87 e 32.35±1.94 g 47.37±1.30 i 28.85±0.93 j
8 Spinach 21.44±0.28 f 40.12±3.26 f 72.58±1.59 e 106.31±1.46 d
9 Horseradish leaves 20.48±0.36 g 45.41±3.71 f 56.99±0.97 g 96.08±0.43 e
10 Carrot 18.86±2.63 g 31.73±1.77 h 59.93±1.58 f 22.33±1.22 l
11 Cabbage (White) 13.95±1.04 h 33.84±2.47 g 52.23±1.47 h 26.24±0.69 k
12 Chili 11.14±1.35 i 58.98±1.36 e 74.20±2.28 e 116.03±2.47 c
13 Leek 5.18±1.29 j 31.13±1.36 g 71.42±1.50 e 90.71±6.91 e
14 Horseradish roots 2.91±0.47 k 4.09±0.21 i 9.23±0.30 k 38.25±2.54 i
15 Lettuce -10.31±0.46 l 3.12±0.28 j 18.94±2.47 j 56.45±0.76 h
16 Cucumber -16.61±1.32m -8.65±0.90 k -6.29±0.88 l 12.38±0.99 m
17 Green pepper -39.73±4.63n -26.88±1.01 l -7.96±1.51 l 73.19±1.38 f

TPh = Total Phenolcis, FW = Fresh weight.

Values(±SD) in the same column followed by the same letter are not significantly different at P<0.05.

Table 3. Relative antioxidant efficiencies of total phenolics in tested vegetables

No Name of vegetable Antioxidant efficiency

50µl 100µl 200µl

1 Parsley 1.00 1.00 1.00

2 Tomato 3.60 2.65 3.35
3 Carrot 3.33 3.06 5.47
4 Yellow onion 3.00 3.01 2.99
5 Red onion 2.84 3.15 3.06
6 Cissus rotundifolia (Halas) 2.63 2.67 2.83
7 Garlic 2.19 2.09 1.99
8 White cabbage 2.10 3.05 4.09
9 Coriander 1.93 1.81 1.65
10 Horseradish leaves 0.84 1.11 1.21
11 Spinach 0.80 0.89 1.39
12 Chili 0.38 1.10 1.30
13 Horseradish roots 0.30 0.25 0.45
14 Leek 0.23 0.81 1.60
15 Lettuce -0.72 0.13 0.68
16 Pepper -2.14 -0.87 -0.22
17 Cucumber -5.29 -1.84 -1.04

The calculated results obtained in Table 3 show that some vegetables such as tomato, carrot,
yellow onion, red onion, garlic and coriander have higher relative antioxidant effeciencies (two-
 Antioxidant Activity of Commonly Consumed Vegetables in Yemen

to five-fold) than that of parsley. On the other hand, other vegetables showed lower relative
antioxidant efficiencies.

DISCUSSION

The results in Table 2 show that the antioxidant activity or prooxidant activity of one or other
types of vegetables either increased or decreased as a function of juice volume. This could be
attributed to an increase in phenolic concentration which leads to an increase in the rate of
reaction. The total phenolic contents were measured in mg /100 g wet weight of the vegetables in
the manner they were purchased and consumed.

The results showed that the antioxidant activities of phenolics in different vegetables varied
markedly (Table 2) and this may be due to the differences in structures of phenolic compounds
and primarily related to their hydroxylation and methylation patterns (Meyer et al., 1998).
Investigation of some common compounds in fruits and vegetables has shown 3,4-dihydroxy
caffeic acid, caftaric, chlorogenic, and neochlorogenic acids to have the highest antioxidant
activities and inhibited LDL oxidation from 86 to 97 % at 5 µM, while ferulic, fertaric, p-
coumaric and p-coutaric acids show lower antioxidant activities (Meyer et al., 1998). However,
esterification to tartaric acid slightly enhance the antioxidant activity of p-coumaric and ferulic
acids (Meyer et al., 1998). Another factor, which may affect the final results of total antioxidant
activity is the lag time (time point where the rate of oxidation reaction increases sharply)
(Vinson et al., 1995a). The increase in lag time could be attributed to the binding of vegetable
phenols with lipoproteins which subsequently protects them from oxidation. Vinson et al.
(1995b) observed an increased LDL + VLDL lag time after spiking with pure polyphenols.
Generally, all compounds tested by Vinson et al. (1995a) produced an increase in lag time with
an increase in concentration. Active compounds exhibited a levelling off of lag time at > 20 µM,
presumably due to saturation of the lipoprotein binding sites (Vinson et al., 1995a). Other
workers found similar results when they studied the effects of different phenolic antioxidants in
inhibition of in vitro human LDL oxidation (Nardini et al., 1995; Pearson et al., 1997). However,
vegetables may contain other antioxidants such as proteins, ascorbate, β-carotene, α-tocopherol,
and lycopene which could play some role in the increase of the total antioxidant activity.
Especially in the case of lycopene, recent studies have shown its potential antioxidant activity as
it almost completely prevented oxidative damage to DNA and liver necrosis in rats (Matos et al.,
2001) and reduced risk of prostate cancer (Giovannucci et al., 2002).

The high antioxidant activities of onions and garlic are in agreement with those results obtained
by Velioglu et al. (1998). Also the pro-oxidant activity of green pepper is similar to that of
yellow bell pepper obtained by Gazzani et al. (1998a). However, the relative increase in
antioxidant activity of tomato compared with the pro-oxidant activity in the study by Gazzani et
al. (1998a), could be attributed to the incubation temperature of the reaction mixture; the
incubation temperature in this study was 37°C instead of 25°C. However, the % antioxidant
activities of tomato, carrot, and cabbage are in agreement with those obtained by the same
auothers in another work carried out under similar conditions (Gazzani et al., 1998b).
 Mohammed Ali Al-Mamary

Phenols belong to a reactive group of compounds that can be attacked by the weak electophile
nitrosonium ion (NO+) and nitrosation may occur easily in aromatic rings bearing more
activating groups such as –OH and –OR attached to them. Therefore, in addition to free radicals
neutralisation, the natural phenolic compounds may play some important role in prevention of
nitrosamines (potent carcinogens) formation which are produced due to the reaction of nitrite
with amines in vivo (R2NH + HONO → R2NN=O + H2O).

The non-linear relationship between the antioxidant activity (AA %) and the total phenolics
obtained in this study indicates that the antioxidant activities of different phenolics may not be
additive as reported elsewhere (Nardini et al., 1995; Pearson et al., 1997; Vinson et al., 1995b).
The high relative antioxidant efficiency values (Table 3) in carrot and tomato compared to
parsley could be due to the quality and not the quantity of the total phenolics which make them
more reactive to neutralise free radicals (Meyer et al., 1998) or may be due to other factors such
as the type of carrotenoids in carrots and tomatoes which show potential antioxidant activity
(Bobeck, 1999; Arab & Steck, 2000; Porrini & Riso, 2000). Significant relative antioxidant
efficiencies in onions, Cissus rotundifolia, garlic, cabbage and coriander could be attributed to
the presence of phenolics as the contents of carrotenoids in onions, garlic and cabbage are very
small compared with those of carrots and tomatoes.

CONCLUSION

High consumption of vegetables containing phenolic antioxidants which inhibit the oxidation of
LDL are said to slow down the process of atherosclerosis and may also reduce the risk of cancer
and other diseases. In the present study, some vegetables such as carrots and tomatoes show the
highest relative antioxiant efficiencies despite the small content of total phenolics. However,
onions, C. rotundifolia, garlic, cabbage and coriander also contain very efficient phenolic
compounds. The present study recommends more consumption of these vegetables that may
have potential health effects. Further work is required to elucidate these results in vivo and to
identify compounds which are responsible for these activities.

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