ARTICLE IN PRESS

Original Article

Variability of carotenes, vitamin C, E and phenolics

in Brassica vegetables
Jagdish Singh, A.K. Upadhyay, Kundan Prasad, Anant Bahadur, Mathura Rai
Indian Institute of Vegetable Research, P.O. Box 5002, P.O. Banaras Hindu University, Varanasi 221 005, Uttar Pradesh, India

Abstract

Antioxidant phytochemicals such as vitamin C, b-carotene, lutein, a-tocopherol, and total phenolics were estimated in fresh samples at the
edible maturity stage in different genotypes of cruciferous vegetables using a reverse-phase HPLC system. Maximum mean vitamin C
(52.9 mg/100 g), b-carotene (0.81 mg/100 g), lutein (0.68 mg/100 g), DL-a-tocopherol content (0.47 mg/100 g) and phenol content (63.4 mg/100 g)
was recorded in broccoli. Results indicate that the cruciferous vegetables are a relatively good source of abundant antioxidants, and there is a
substantial and signicant variation, both within and between the subspecies, for the antioxidant phytochemicals.

Keywords: Vitamin C; b-carotene; Lutein; DL-a-tocopherol; Total phenolics; Antioxidant phytochemicals; Brassica vegetables

1. Introduction noids, vitamins E and C are now rmly established as

Many Brassicaceae crops (e.g., broccoli, Brussels
sprouts, cabbage, cauliower), commonly known as
crucifers, are widely recognized for their contribution to
human nutrition and for other health benets (Salunkhe
and Kadam, 1998). A diet rich in cruciferous vegetables has
been associated with inhibitions of chemically induced
carcinogenesis in laboratory animals and humans (Kushad
et al., 1999). Numerous studies have indicated that the
hydrolytic products of some of the glucosinolates have
anticarcinogenic activity (Stoewsand, 1988). Another
group of cancer-ghting substances in foods are the
vitamin antioxidants. These antioxidants such as carotenes,
DL-a-tocopherol and ascorbate have also been associated
with a reduced risk of cardiovascular diseases and several
types of cancer (Byers and Perry, 1992). Signicant
variations in carotenoids, ascorbate, tocopherols, glucosi-
nolates and myrosinase activity among cruciferous
genotypes and within each genotype suggest differences
in the health-promoting properties of these vegetables
(Kushad et al., 1999; Kurilich et al., 1999). The carote-
protective dietary antioxidants (Sies and Stahl, 1995).
DL-a-tocopherol, the most common form of vitamin E is
most biologically active (Bjorneboe et al., 1990). Poly-
phenols and avonoids are also gaining prominence
(Cao et al., 1997). Members of the Brassica family of
vegetables have signicant cancer-preventive properties
(Verhoeven et al., 1997). The potential protective role of
cruciferous vegetables and active components present in
these vegetables, such as isothiocyanates and indole-3-
carbinol, has been extensively studied in experimental in
vitro and in vivo carcinogenesis models. Studies have
shown that people who consume these vegetables fre-
quently have a lower risk of developing a variety of
cancers, including cancers of the colon, stomach and lung.
Finally, research is uncovering that many of these
phytonutrients act synergistically (Palozza and Krinsky,
1992). Although some studies on the estimation of these
primary antioxidants have been carried earlier (Hart and
Scott, 1995; Kurilich et al., 1999; Booth and Bradford,
1963), no systematic study has been conducted on the
broad range of Indian cultivars.
There is a need for quantitative data on the antioxidant
content of various subspecies of Brassica vegetables. Such
information will not only increase the understanding of the
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function of these antioxidant phytochemicals in lowering
incidence of aging and other chronic diseases, but the
studies related to qualitative and quantitative distribution
of primary antioxidants in cruciferous vegetables may also
help in breeding programmes to develop new germplasm
with a high content of such phytochemicals. The objective
of this paper is to provide new data based on HPLC
estimations regarding the antioxidant content of Brassica
vegetables.
2. Materials and methods
The replicated eld trial was carried out at the research
farm of IIVR, Varanasi, Uttar Pradesh, India, with
standard agricultural practices. A disease-free, healthy
crop was cultivated and, at the edible maturity stage, three
uniform-size plants, free of insect and/or physical damage
were selected from each species to constitute replicates. The
edible portions of cabbage (Brassica oleracea. L. var.
capitata), Chinese cabbage (Brassica rapa L. pekinensis
(Lour.) Olsson), cauliower (Brassica oleracea L. var.
botrytis), broccoli (Brassica oleracea L. var. italica Plenck.)
and Brussels sprouts (Brassica oleracea L. var. gemmiferae
Zenk.) were harvested and immediately transferred to the
laboratory. Sub-samples of 100 g each per replicate per
plant were combined, weighed and utilized for further
analyses. Three independent samples were analyzed for
each accession and values reported are the mean of three
different determinations. For identication and quantica-
tion of L-ascorbic acid, b-carotene, lutein (lutein:
a-carotene-3, 30 -diol) the standards were purchased from
Sigma Chemical Co., St. Louis, MO, USA and for
DL-a-tocopherol the standards were purchased from
Merck, Dermstadt, Germany. The compound identica-
tion was based on retention time of known standards. The
recoveries were 9294% for b-carotene, 90% for lutein,
and 7779% for a-tocopherol. The phytochemicals were
quantied by the procedure of Kurilich et al. (1999) on a
Shimadzu HPLC system equipped with DGU-14A
Degasser, LC-10AT quaternary pump, and SPD-10AV
UVVisible detector. Separations were performed on a
Phenomenexs C18 reverse-phase column (5 mm;
150  4.6 mm i.d.). The column was protected by a
Phenomenexs C18 (5 mm; 4 mm  3 mm i.d.) guard
cartridge.
2.1. Analysis of vitamin C
Ten grams of fresh tissue was homogenized in a Waring
blender with 100 mL of 1% m-phosphoric acid. The slurry
was adjusted to 250 mL with 1% m-phosphoric acid and
ltered through Whatman lter paper. One milliliter of this
ltrate was added to 1.0 mL of 5% dithiothreitol, and the
volume was made up to 10 mL with 1% m-phosphoric acid.
The solution was ltered on a 0.2 mm nylon lter and 10 mL
was injected on a reverse phase C-18 (150  4.60 mm 5 mm)
HPLC column. The mobile phase consisted of acetonitrile:
0.05 M KH2PO4 (pH 5.9) in the ratio of 75:25 with a ow
rate of 1.5 mL/min. The sample was detected at 261 nm on
a Shimadzu SPD-10AV, UVVisible detector. The reten-
tion time for standard vitamin C was recorded as
2.565 min.
2.2. Analysis of b-Carotene and lutein
b-Carotene and lutein were extracted and analyzed
according to the procedure published by Kurilich et al.
(1999). One hundred milligrams of sample was put into a
test tube and 10 mL of ethanol containing 0.1 g of BHT
were added. The test tube with the sample was placed in a
water bath at 700 1C for 15 min. After removing the tubes
from the water bath, the tissue was completely homo-
genized in a mortar and ltered through Whatman no. 42
lter paper. Then 180 mL of 80% KOH was added to each
tube. The sample was then saponied at 70 1C for 30 min.
Saponication was done to remove chlorophyll and other
lipids. The samples were placed directly in an ice bath, and
2.5 mL of de-ionized water and 2.5 mL hexane: toluene
mixture (10:8) was added. Then the tubes were vortexed
and centrifuged at 2100 rpm for ve minutes. The upper
layer hexane:toluene fraction was then transferred to a
separate test tube. The hexane:toluene extraction was
repeated two more times. The combined hexane:toluene
fractions were dried using a Speed-vac concentrator. The
residue was reconstituted in 200400 mL THF. The solution
was ltered on a 0.2 mm nylon lter and 20 mL of the ltered
solution was injected in the Shimadzu High performance
liquid chromatograph. The mobile phase consisted of
acetonitrile:methanol:THF (52:40:8) (v/v/v) at a ow rate
of 0.7 mL/min. The absorbance was recorded at 450 nm for
b-carotene and lutein, respectively. The retention time for
the standard b-carotene was recorded as 6.192 min and
for lutein at 2.35 min.
2.3. Estimation of DL-a-tocopherol
The extraction method used for DL-a-tocopherol
was similar to the method described for carotenoids;
however, the absorbance was measured at 295 nm for
DL-a-tocopherol estimation. The retention time for stan-
dard DL-a-tocopherol was 9.067 min. The concentration
was calculated from the peak area and was corrected for
percent recovery.
2.4. Estimation of total phenolics
Total phenolics were determined using the Folin
Ciocalteu reagent (Singleton and Rossi, 1965). Samples
(2 g) were homogenized in 80% aqueous ethanol at room
temperature and centrifuged in cold at 10 000 rpm for
15 min at 4 1C and the supernatant was preserved. The
residue was re-extracted twice with 80% ethanol and
supernatants were pooled and evaporated to dryness at
room temperature. Residue was dissolved in 5 mL of
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distilled water. One hundred microliter of this extract was
diluted to 3 mL with water and 0.5 mL of FolinCiocalteu
reagent was added. After 3 min, 2 mL of 20% of sodium
carbonate was added and the contents were mixed
thoroughly. The color was developed and absorbance
measured at 650 nm in a UV-1601 Shimadzu spectro-
photometer after 60 min using gallic acid as a standard.
The results were expressed as mg gallic acid equivalents per
100 g fresh weight.
Recovery experiments were performed in triplicate from
plant homogenates of each replication, spiked with known
concentrations of standard solutions during the extraction.
The mean values for the recoveries were 92%, 87%, 96%
and 81% for vitamin C, DL-a-tocopherol, b-carotene lutein
and phenols, respectively. The values reported were then
modied accordingly, based on the percent recovery.
2.5. Statistical analysis
The analysis of variance was performed on data for
differences between and within the subspecies using the
ANOVA (SPSS Ver. 10). Mean separations were deter-
mined by least signicant difference (LSD) at P p0.05%.
3. Results and discussion
Cabbage: Eighteen different cultivars of cabbage were
assayed for variability between the cultivars for the
antioxidant phytonutrients. Data presented in Table 1
show that the vitamin C content ranged from 5.7 to
23.5 mg/100 g. The maximum vitamin C content was
recorded in cultivar Sprint ball (23.5 mg/100 g), followed
by Gungaless (12.9 mg/100 g). The minimum vitamin C
content was recorded in cultivar Kirch-11 (5.7 mg/100 g),
followed by Golden Acre (5.8 mg/100 g). The b-carotene
content in cabbage ranged from 0.01 to 0.12 mg/100 g. The
maximum b-carotene content was recorded in Quisto
(0.12 mg/100 g) followed by Green Challenger and Rare
Ball (0.11 mg/100 g). The minimum value for b-carotene
was noted in cultivar Pusa Mukta (0.01 mg/100 g). Lutein
content was also recorded in the cabbage cultivars, which
ranged from 0.02 to 0.26 mg/100 g. Maximum lutein
content was recorded in Quisto (0.26 mg/100 g) and minimum
in Pusa Mukta (0.02 mg/100 g). The values for b-carotene
and lutein reported in this study are lower than the earlier
report of Takagi (1985) for b-carotene (3.09 mg/100 g)
and lutein content (6.28 mg/100 g) in cabbage, respectively.
Vitamin E (DL-a-tocopherol) was estimated only in fourteen
cabbage cultivars, which ranged from 0.03 to 0.20 mg/100 g.
Maximum DL-a-tocopherol content was recorded in
Rare Ball (0.20 mg/100 g) and minimum in Green Cornell
(0.03 mg/100 g). The DL-a-tocopherol values in cabbage
cultivars are in agreement with the earlier report of
Ching and Mohamed (2001), in which the DL-a-tocopherol
value in cabbage on fresh weight basis was reported to
be 0.69 mg/100 g. Total phenol content was also estimated
only in 14 cultivars and the values ranged from 12.6 to
34.4 mg/100 g. Signicant variation in the phenolic

Table 1
Antioxidant phytonutrients (mean and ranges) in 18 cabbage cultivars

Cabbage cultivars Vitamin C b-Carotene Lutein DL-a-tocopherol Phenolics

Gungaless 12.9b 0.02ij 0.03i 0.16bc 15.4def

Pusa Mukta 10.8c 0.01k 0.02i 0.06ef 12.6f
Kirch-10 6.86fg 0.06d 0.15e 0.03g 18.1d
Kirch-11 5.66g 0.08c 0.12g 0.04fg
Sprint Ball 23.5a 0.03hi 0.11g 0.05efg
T-676 8.19ef 0.02jk 0.03i 0.06e
Golden Cross 10.3cd 0.03gh 0.07h 0.12d
Resist Crown 9.90cde 0.02ijk 0.03i 0.17b 27.1c
Golden Acre 5.85g 0.06d 0.22bc 0.14c 13.1ef
Quisto 10.7c 0.12a 0.26a 0.05efg 31.0b
Rare Ball 8.48ef 0.11b 0.13f 0.20a 18.2d
Mini Ball 10.8c 0.03hi 0.22bc 16.4de
Hari Rani Gol 8.60def 0.04fg 0.21c 0.04fg 15.1def
Fieldman 7.37fg 0.05de 0.12fg 0.03g 18.7d
Green Cornell 5.96g 0.04ef 0.11g 0.03g 34.4a
Green Yogendra 9.97cde 0.03hi 0.19d 15.7def
Green Challenger 8.96cdef 0.12b 0.23b 13.7ef
BC-76 8.86cdef 0.04ef 0.22bc 12.9ef
Range 5.6623.5 0.010.12 0.020.26 0.030.20 12.634.4
Mean 9.65 0.05 0.14 0.08 18.7
CD at 5% 1.90 0.01 0.01 0.02 3.29
S.D. 4.14 0.04 0.08 0.06 7.01

All values are reported in mg/100 g fresh weight.

Each mean represents analyses of three independent samples.
Different letters indicate signicant differences within columns by Duncans test at P p0.05.
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Table 2
Antioxidant phytonutrients in two cauliower cultivars

Cauliower cultivars Vitamin C b-Carotene Lutein DL-a-tocopherol Phenolics

Snow Ball-16 13.8b 0.10a 0.15a 0.22a 21.8a

Kanchan 24.8a 0.05b 0.11a 0.08b 16.3a
Mean 19.3 0.08 0.13 0.15 19.1
CD at 5% 1.00 0.01 0.05 0.06 8.3
S.D. 6.35 0.03 0.02 0.07 3.42

All values are reported in mg/100 g fresh weight.

Each mean represents analyses of three independent samples.
Different letters indicate signicant differences within columns by Duncans test at P p 0.05.

Table 3
Antioxidant phytonutrients in two Brussels sprouts cultivars

Brussels sprout cultivars Vitamin C b-Carotene Lutein DL-a-tocopherol Phenolics

Diablo 17.0a 0.15a 0.45a 0.14a 35.0b

Hilds Ideal 14.6a 0.13b 0.40b 0.16a 40.4a
Mean 15.8 0.14 0.43 0.15 37.7
CD at 5% 11.7 0.001 0.03 0.02 2.21
S.D. 2.49 0.02 0.06 0.02 4.51

All values are reported in mg/100 g fresh weight.

Each mean represents analyses of three independent samples.
Different letters indicate signicant differences within columns by Duncans test at P p0.05.

content was observed in different accessions of cabbage
(Pp0.05). The range for total phenolic content in
cabbage cultivars recorded in this study are lower than the
previously published data of Chu et al. (2002), wherein
they reported higher total phenolic content in cabbage
(54.6 mg/100 g). Miller et al. (2000) studied the antioxidant
activity of different vegetables and noticed striking difference
between red and green cabbage. Apparently, the purple
cabbage pigment contributes a high level of antioxidant
activity.
Cauliflower: In cauliower the vitamin C content was
signicantly higher in cultivar Kanchan (24.8 mg/100 g) as
compared to Snow Ball-16 (13.8 mg/100 g; see Table 2).
In contrast to this, cultivar Snow Ball-16 had higher
b-carotene content (0.10 mg/100 g) as compared to
Kanchan (0.05 mg/100 g). Comparatively there was
less variation for the lutein content among the two
cultivars. Snow Ball-16 had slightly higher lutein content
(0.15 mg/100 g) as compared to Kanchan (0.11 mg/100 g).
Regarding vitamin E content, signicant difference
between the two cultivars was observed and Snow
Ball-16 had signicantly higher DL-a-tocopherol content
(0.22 mg/100 g) in comparison to Kanchan (0.08 mg/100 g).
Kurilich et al. (1999) reported the b-carotene, DL-a-
tocopherol and ascorbate content in cauliower accessions
to be in the range of 0.070.08 mg/100 g, 0.161.20 mg/100 g,
and 39.644.3 mg/100 g, respectively. Phenolic content was
higher in Snow Ball-16 (21.8 mg/100 g) in comparison to
Kanchan (16.3 mg/100 g) but the difference was not signi-
cant (P0.05 8.32).
Brussels sprouts: Two cultivars of Brussels sprouts,
namely Diablo and Hilds Ideal, were analyzed. The data
presented in Table 3 revealed that in the two test cultivars,
mean vitamin C and E content was recorded as 15.8 mg/100 g
and 0.15 mg/100 g, respectively, but the two test cultivars did
not differ signicantly with respect to vitamin C or DL-a-
tocopherol; however, signicant differences were recorded
among the cultivars for b-carotene (P0.05 0.01), lutein
(P0.05 0.03) and phenolics (P0.05 2.21).
Chinese cabbage: The antioxidant phytonutrients
were also estimated in four Chinese cabbage accessions
(Table 4). The vitamin C content in Chinese cabbage
ranged from 5.62 to 12.6 mg/100 g. Maximum vitamin
C content was recorded in cultivar CCSH-1 and mini-
mum in Optico. CCLH-1 had the maximum b-carotene
(0.03 mg/100 g), lutein (0.04 mg/100 g) and DL-a-tocopherol
content (0.10 mg/100 g). The maximum phenolic content
was recorded in Solan Band Sarson (13.7 mg/100 g),
while CCSH-1 recorded the minimum phenolic content
(5.10 mg/100 g).
Broccoli: Six different accessions of broccoli were
analyzed for the major antioxidant phytochemicals (Table 5).
The vitamin C content in broccoli ranged from 25.5
to 82.3 mg/100 g. Maximum vitamin C content was recorded
in NS-50 (82.3 mg/100 g); however, Lucky had the mini-
mum vitamin C content (25.5 mg/100 g). The b-carotene
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Table 4
Antioxidant phytonutrients (mean and ranges) in four Chinese cabbage cultivars

Chinese cabbage cultivars Vitamin C b-Carotene Lutein DL-a-tocopherol Phenolics

CCSH-1 12.6a 0.01b 0.01c 0.07b 5.10d

CCLH-1 11.6ab 0.03a 0.04a 0.10a 9.44c
Solan Band Sarson 8.9b 0.01c 0.01c 0.06b 13.7a
Optico 5.6c 0.01c 0.02b 0.07b 11.5b
Range 5.62.6 0.010.03 0.010.04 0.060.10 5.113.7
Mean 9.71 0.01 0.02 0.08 9.93
CD at 5% 2.74 0.04 0.01 0.01 1.05
S.D. 3.17 0.01 0.01 0.01 3.6

All values are reported in mg/100 g fresh weight.

Each mean represents analyses of three independent samples.
Different letters indicate signicant differences within columns by Duncans test at P p 0.05.

Table 5
Antioxidant phytonutrients (mean and ranges) in six broccoli accessions

Broccoli cultivars Vitamin C b-Carotene Lutein DL-a-tocopherol Phenolics

Solan green 58.7b 1.13a 1.02a 0.22d 62.9c

NS-50 82.3a 0.90b 0.77b 0.45c 66.4bc
Hyb. No.-2 53.6c 0.80d 0.71b 0.44c 44.5e
Fiesta 43.4d 0.48f 0.41c 0.48bc 52.2d
Sultan 53.6c 0.85c 0.77b 0.68 a 82.9a
Lucky 25.5e 0.70e 0.43c 0.55b 71.2b
Range 25.582.3 0.481.13 0.411.02 0.220.68 44.582.9
Mean 52.9 0.81 0.68 0.47 63.4
CD (5%) 4.22 0.01 0.10 0.07 5.4
S.D. 17.7 0.20 0.22 0.14 13.1

All values are reported in mg/100 g fresh weight.

Each mean represents analyses of three independent samples.
Different letters indicate signicant differences within columns by Duncans test at P p0.05.

and lutein content in broccoli cultivars ranged from 0.48 to
1.13 mg/100 g and from 0.41 to 1.02 mg/100 g, respectively.
Yang and Henze (1988) reported the b-carotene and
lutein content of broccoli cultivars as 2.58 mg/100 g and
4.0 mg/100 g, respectively. Lutein, in particular, is believed
to be able to increase the density of the macular pigment in
the eye and may reduce the risk of age related macular
degeneration. The vitamin E content in broccoli cultivars
ranged from 0.22 to 0.68 mg/100 g. Maximum DL-a-
tocopherol content was recorded in cultivar Sultan
(0.68 mg/100 g). The DL-a-tocopherol values obtained in this
study are lower than that of Ching and Mohamed
(2001) (2.9570.10 mg/100 g); however, the values are in close
agreement to those of Bauernfeind, (1980) (0.50 mg/100 g).
The phenolic content was also comparatively higher in broccoli
cultivars and the values ranged from 44.5 to 82.9 mg/100 g.
Maximum phenolic content was recorded in cultivar Sultan
(82.9 mg/100 g) and minimum in Hybrid No. 2 (44.5 mg/100 g).
The values for phenolics are close to previously published
result of Chu et al. (2002), who studied the complete
prole of phenolic distributions of 10 common vegetables
and reported that broccoli possessed the highest total phenolic
content (101.671.24 mg/100 g).
The mean data of the antioxidant phytonutrients
in the edible tissues of different subspecies of Brassica
oleracea is summarized in Table 6. Maximum mean
vitamin C (52.9 mg/100 g), b-carotene (0.81 mg/100 g),
lutein (0.68 mg/100 g), DL-a-tocopherol (0.47 mg/100 g)
and phenolic content (63.4 mg/100 g) were recorded in
broccoli. The statistical analysis of the relationship between
total phenolic content and anti-oxidant activity of
vegetables showed a positive and highly signicant
relationship (r2 0.6578, Po0.005) (Kaur and Kapoor,
2002). Chu et al. (2002) observed that, although there
is a positive correlation between antioxidant activity
and free phenolic content, the correlation was not
strong (r2 0.69). The values for DL-a-tocopherol and
ascorbate reported in this study are generally in accordance
with those of previous reports (Kurilich et al., 1999;
Bauernfeind, 1980). The range for b-carotene is also close
to the previously published data of Kurilich et al. (1999)
and Khachik et al. (1986), who reported the b-carotene
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Table 6
Antioxidant phytonutrients in edible tissues of Brassica oleracea subspecies

Brassica oleracea subspecies Vitamin C b-Carotene Lutein DL-a-tocopherol Phenolics

Chinese cabbage 9.71d 0.01c 0.02d 0.08c 9.93d

Cauliower 19.3b 0.08bc 0.13c 0.15b 19.1c
Cabbage 9.66d 0.05c 0.14c 0.08c 18.7c
Brussels Sprouts 15.8c 0.14b 0.43b 0.15b 37.7b
Broccoli 52.9a 0.81a 0.68a 0.47a 63.4a
CD at 5% 3.35 0.06 0.05 0.02 7.61
S.D. 17.0 0.31 0.25 0.15 20.0

All values are reported in mg/100 g fresh weight.

Each mean represents analyses of three independent samples.
Different letters indicate signicant differences within columns by Duncans test at Pp0.05.

content of broccoli (0.48 mg/100 g), cabbage (0.08 mg/100 g),
and Brussels sprouts (0.53 mg/100 g). However, Herrmann
(1975) reported the range for b-carotene content in broccoli
(0.132.40 mg/100 g), Brussels sprouts (0.150.70 mg/100 g),
green cabbage (0.907.58 mg/100 g) and Kohlrabi
(0.150.45 mg/100 g).
The variations in the values of antioxidant phytochem-
icals as observed in the present study and earlier reports
may be due to several factors, including genetic and
environmental inuences, as well as the differences in the
methods of estimation. Another important source of
variation may be the harvesting stage of the samples.
Results indicate that the cruciferous vegetables are
relatively good sources of abundant antioxidants, and
there is a substantial and signicant variation, both within
and between the subspecies for the antioxidant phyto-
chemicals. The substantial difference in the antioxidant
phytochemicals within the subspecies indicates that the
potential health benets also depend on the genotype. The
results demonstrate the potential value of cruciferous
vegetables as a dietary source of antioxidants.
Acknowledgements
The authors are grateful to Dr. G. Kalloo, Deputy
Director General (Hort. and Crop Sciences), Indian
Council of Agricultural Research, for providing nancial
assistance for this ad hoc project from AP-Cess funds of
Horticulture Division, ICAR, New Delhi, India.
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