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Brassica genus includes known horticultural vegetables with major economical importance worldwide, and involves vegetables of economical importance being part of the diet and source of oils for industry in many countries. Brassicales own a broad array of health-promoting compounds, emphasized as healthy rich sources of vitamin C. The adequate management of pre- and postharvest factors including crop varieties, growth conditions, harvesting, handling, storage, and final consumer operations would lead to increase or preserve of the vitamin C content or reduced losses by interfering in the catalysis mechanisms that remains largely unknown, and should be reviewed. Likewise, the importance of the food matrix on the absorption and metabolism of vitamin C is closely related to the range of the health benefits attributed to its intake. However, less beneficial effects were derived when purified compounds were administered in comparison to the ingestion of horticultural products such as Brassicas, which entail a closely relation between this food matrix and the bioavailability of its content in vitamin C. This fact should be here also discussed. These vegetables of immature flowers or leaves are used as food stuffs all over the world and represent a considerable part of both western and non-Western diets, being inexpensive crops widely spread and reachable to all social levels, constituting an important source of dietary vitamin C, which may work synergistically with the wealth of bioactive compounds present in these foods.
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Brassica Foods as a Dietary Source of Vitamin C: A
Review
R. Domínguez-Perles a , P. Mena a , C. García-Viguera a & D. A. Moreno a
a Phytochemistry Lab. Department of Food Science and Technology , Centro de Edafología y
Biología Aplicada del Segura-Consejo Superior de Investigaciones Científicas (CEBAS-CSIC) ,
Espinardo , Murcia, 30100 , Spain
Accepted author version posted online: 26 Mar 2013.Published online: 05 Feb 2014.
To cite this article: R. Domínguez-Perles , P. Mena , C. García-Viguera & D. A. Moreno (2014) Brassica Foods as
a Dietary Source of Vitamin C: A Review, Critical Reviews in Food Science and Nutrition, 54:8, 1076-1091, DOI:
10.1080/10408398.2011.626873
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Critical Reviews in Food Science and Nutrition, 54:1076–1091 (2014)
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Taylor and Francis Group, LLC
ISSN: 1040-8398 / 1549-7852 online
DOI: 10.1080/10408398.2011.626873
Brassica Foods as a Dietary Source
of Vitamin C: A Review
R. DOM´
INGUEZ-PERLES,*P. MENA,*C. GARC´
IA-VIGUERA,
and D. A. MORENO
Phytochemistry Lab. Department of Food Science and Technology. Centro de Edafolog´
ıa y Biolog´
ıa Aplicada del
Segura-Consejo Superior de Investigaciones Cient´
ıficas (CEBAS-CSIC), Espinardo, Murcia 30100, Spain
Brassica genus includes known horticultural vegetables with major economical importance worldwide, and involves veg-
etables of economical importance being part of the diet and source of oils for industry in many countries. Brassicales own
a broad array of health-promoting compounds, emphasized as healthy rich sources of vitamin C. The adequate manage-
ment of pre- and postharvest factors including crop varieties, growth conditions, harvesting, handling, storage, and final
consumer operations would lead to increase or preserve of the vitamin C content or reduced losses by interfering in the
catalysis mechanisms that remains largely unknown, and should be reviewed. Likewise, the importance of the food matrix
on the absorption and metabolism of vitamin C is closely related to the range of the health benefits attributed to its intake.
However, less beneficial effects were derived when purified compounds were administered in comparison to the ingestion of
horticultural products such as Brassicas, which entail a closely relation between this food matrix and the bioavailability of
its content in vitamin C. This fact should be here also discussed.
These vegetables of immature flowers or leaves are used as food stuffs all over the world and represent a considerable part
of both western and non-Western diets, being inexpensive crops widely spread and reachable to all social levels, constituting
an important source of dietary vitamin C, which may work synergistically with the wealth of bioactive compounds present in
these foods.
Keywords Vitamin C, Brassica, ascorbic acid, dehydroascorbic acid, pre-harvest, post-harvest, bioavailability, health
1. INTRODUCTION
The Brassicaceae crop plants (broccoli, cauliflower, Brussels
sprouts, cabbages, turnips, etc.) are food staples used world-
wide (Figure 1) and represent a considerable portion of human
diet (Vallejo et al., 2002b; Jahangir et al., 2009; Kusznierewicz
et al., 2010). A broad array of healthy properties have been
attributed to Brassica species in recent years; such as anticar-
cinogenic, protective actions against cardiovascular diseases and
ageing processes, prenatal pathologies, cataracts, etc. (Kataya
and Hamza, 2008; Kim et al., 2008; Tiku et al., 2008; Ja-
hangir et al., 2009; Akhlaghi and Bandy, 2010; Emmert et al.,
2010). These benefits have been related to their high content in
Address correspondence to D. A. Moreno, Phytochemistry Lab. Depart-
ment of Food Science and Technology. Centro de Edafolog´
ıa y Biolog´
ıa Apli-
cada del Segura-Consejo Superior de Investigaciones Cient´
ıficas (CEBAS-
CSIC), Post Office Box 164, Espinardo, Murcia 30100, Spain. E-mail:
dmoreno@cebas.csic.es
These two authors have contributed equally to the present work.
health-promoting phytochemicals namely: glucosinolates (and
their hydrolysis products, isothiocianates), phenolic compounds
(hydroxycinamic acids and flavonoids), carotenoids, vitamins
(ascorbic acid (AA), tocopherol, and folic acid), and minerals
(Vallejo et al., 2002a; Heimler et al., 2006; Fernandes et al.,
2007; Ferreres et al., 2009; Taveira et al., 2009; Dom´
ınguez-
Perles et al., 2010; Yang et al., 2010; P´
erez-Balibrea et al.,
2011). Regardless of the rich profile in bioactive compounds of
Brassica genus, current trials are focused on the potential role
of isolated phytochemicals, including vitamin C, largely known
as essential nutrient, that lacks an integrative approach to un-
derstand its functions on health along with the rest of bioactive
constituents in their natural food concentrations and the condi-
tioning of the food matrix on its bioavailability (Blot et al., 1993;
Loria et al., 2000; Bjelakovic et al., 2007; Li and Schellhorn,
2007a; Frei and Lawson, 2008; Kim et al., 2008). Actually, it
should be taken into account that Brassicas generally contain
high amounts of vitamin C, even though the traditional source
has also been the Citrus family. In fact, depending on consumer
habits of different countries, Brassica vegetables can provide
the 50% of the daily recommended dietary intake of vitamin C,
1076
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BRASSICA FOODS AS A DIETARY SOURCE OF VITAMIN C 1077
Figure 1 Vernacular and scientific names of some examples of commercial Brassicaceae.
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1078 R. DOM´
INGUEZ-PERLES ET AL.
leading the sources of natural vitamin C for human populations
(Pennington and Fisher, 2010).
Therefore, the aim of this review was to describe the existing
variations in the contents of vitamin C among Brassica species,
pointing out the effects of the preharvest (specie, variety, organ,
and developmental stage) and postharvest (handling, storage,
and processing procedures) on this nutrient for high quality
commodities. The relevance of the health benefits attributed to
vitamin C derived from the Brassica consumption as affected
by the food matrix, as well as its absorption and metabolism,
will also be discussed.
2. PREHARVEST CONDITIONS AFFECTING VITAMIN
C CONTENT IN BRASSICA FOODS
The capital relevance of preharvest factors on the nutritional
quality of Brassica foods has been widely reported and it is
clear that the adequate management of the production factors
affecting the plant growth may help to increase their content
in bioactive compounds at harvest, not only by selecting the
best species and varieties for any specific production area, but
also by optimizing the growing conditions of the selected crops.
Therefore, among the different preharvest factors conditioning
the vitamin C content of Brassica vegetables, two groups could
be established. First, those factors inherent to the considered
crop: genetic (species and cultivars) and physiological factors
(organ and developmental stage), as “internal” factors. In this
sense, the second group would include all the “external” fac-
tors including the environmental and agronomic conditions and
practices harvesting and handling procedures.
2.1. Genetic Information
The major inherent internal factor to crucifers is the large
variation among genotypes, and a good example can be found-
ing Brassica genus (Table 1), for vitamin C concentrations
ranging up to fourfold differences among species: broccoli (B.
oleracea var. italica), Brussels sprouts (B. oleracea var. gem-
mifera), kale (B. oleracea var. acephala), and mustard spinachs
(B. rapa var. perviridis), exhibing higher contents (100, 107,
118, and 130 mg of vitamin C per 100 g fw on average, respec-
tively), widely surpassed the black mustards (B. nigra), canola
(B. napus), cauliflower (B. oleracea var. botrytis), collards (B.
oleracea var. viridis), Indian mustards (B. juncea var. rugosa),
turnips (B. rapa vars. rapifera and rapa), and cabbages (B. ol-
eracea var. capitata,B. rapa var. chinensis,var.parachinensis,
and var. pekinensis) that presented ranging 35–68 mg 100 g1
fw (Table 1). Data of the variation of vitamin C contents of dif-
ferent Brassica species analyzed under equal conditions have
been published by the United States Department of Agriculture
(USDA), confirming this fact under the minimized influence of
the analytical method (USDA, 2010).
Penintong et al. cited an alternative classification that showed
collards, kale, turnip greens, and mustards as the Brassicas with
the highest contents in vitamin C in comparison with broc-
coli, Brussels sprouts, cabbage, cauliflower, Chinese broccolis,
and Chinese cabbages (Pennington and Fisher, 2010). In earlier
works, the lowest values have been registered for some varieties
of cabbage (5.7–25.3 mg 100 g1fw (Singh et al., 2007)). Addi-
tionally, the comparison of the content of vitamin C in separate
cultivars belonging to the same species has shown differences
of up to 5% for broccoli, 3.7% for kale, 2.7% for collards,
2% for cauliflower, Indian mustards, cabbage, and turnips, and
1.5% for Brussels sprouts and Chinese cabbage (Table 1). The
variation in the content of vitamin C among Brassicaceae mem-
bers has been attributed to their inherent genetic background,
while minor changes could be also attributed to differences in
the experimental procedures or analytical methods. In addition,
the fact that the species most widely integrated in the market
and human consumption habits (broccoli, kale, collards, and
cauliflower), and therefore, which are subjected to more intense
genetic breeding showed also the strongest variation, linking
the genetic factor as responsible of the variation in their vitamin
C contents. Furthermore, the experimental procedures in which
variations in the analytical and storage conditions, represent a
factor with marginal relevance, give additional support to the
critical effect of the genetic influence on the vitamin C content
in Brassica spp., with variations of up to 54% for broccoli, 12%
for cauliflower, and 32% for cabbage (Kurilich et al., 1999;
Ferreres et al., 2006; Vrchovsk´
a et al., 2006; Borowski et al.,
2008; Sousa et al., 2008). In this sense, Vallejo et al., analyzed
the content in vitamin C of 14 breeding and commercial broc-
coli varieties recording differences of up to 71% (Vallejo et al.,
2002b), even though they were grown, processed, and analyzed
under equal conditions, suggesting again the major relevance
of the genetics and breeding in determining the Brassicas load
of dietary vitamin C over the distinct experimental conditions.
Despite the existing variations in vitamin C contents in Bras-
sicas, we emphasize that the natural foods of this genus are a
good source of vitamin C among a broad array of fruits and
vegetables.
2.2. Organ and Developmental Stage
Other group of inner factors; including the physiological ef-
fects of the distinct plant organs, or the developmental stage
at harvest, are also critical for the nutrient contents of fruits
and vegetables. Considering broccoli as a model because of its
intense characterization and interest as commercial Brassica,
significant changes occurred on vitamin C levels through its
development, as for other bioactives. While in broccoli seeds,
vitamin C is almost undetected, a progressive increase of the
vitamin C in broccoli sprouts was described from 3 to 12 days
of age (P´
erez-Balibrea et al., 2008; P´
erez-Balibrea et al., 2010).
Later on, in adult plants during flowering, the vitamin C accumu-
lation in broccoli inflorescences from the early flower bottom
to the mature head reached even a fivefold increased amount
(Omary et al., 2003; Vallejo et al., 2003a). Another remarkable
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BRASSICA FOODS AS A DIETARY SOURCE OF VITAMIN C 1079
Tab l e 1 Content in vitamin C (mg 100 g1fw) of fresh edible parts of Brassica plants
Commodity AA Vitamin C Extraction/analysis method Source (Reference)
Broccoli (Brassica oleracea var.
italica)
93.2 Total ascorbic acid (USDA, 2010)
83.0 Trichloroacetic acid/HPLC (Puupponen-Pimi¨
a et al., 2003)
66.4 Till-mans method (Sikora et al., 2008)
72.2–122.6 MeOH:H2O/HPLC (Vallejo et al., 2003b)
37.7–124.9 (Vallejo et al., 2003a)
200 (L´
opez-Berenguer et al., 2007)
115 (leaves) (L´
opez-Berenguer et al., 2009)
150 (L´
opez-Berenguer et al., 2009)
106.9 117.7 MeOH:H2O/HPLC (Vallejo et al., 2002a)
130 (Moreno et al., 2007a)
25.5–82.3 Nonavailable (Jagdish et al., 2006)
84 Citric acid/HPLC (Hrncirik et al., 2001)
77–93 Methaphosphoric
acid/2,6-Dichloroindophenol
(Favell, 1998)
74.8 (Bahorun et al., 2004)
96.79 (Schonhof et al., 2007)
32 (Ansorena et al., 2011)
2.34–5.77Metaphosphoric acid/microfluorometric
method
(Borowski et al., 2008)
112 (78 stems) Metaphosphoric acid/spectophotometry (Murcia et al., 2000)
89.0–148.2 97.0–163 Methaphosphoric acid/HPLC (Vanderslice et al., 1990)
121.1 (Mangels et al., 1993)
74.7 (Kurilich et al., 1999)
152 (Howard et al., 1999)
75 (Hussein et al., 2000)
43.2–146.3 (Vallejo et al., 2002b)
103 (124 stems) (Zhang and Hamauzu, 2004)
41–64 (Franke et al., 2004)
87.19 (Koh et al., 2009)
374.1 (Patras et al., 2011)
113 Not available (Davey et al., 2000)
93 (Chu et al., 2002)
35–65 (Lemoine et al., 2010)
Broccoli raab (Brassica rapa
var. ruvo)
20.1 Total ascorbic acid (USDA, 2010)
26.6 MeOH:H2O/HPLC (Cefola et al.)
Brussels sprouts (Brassica
oleracea var. gemmifera)
85 Total ascorbic acid (USDA, 2010)
90.3 Till-mans method (Sikora et al., 2008)
27.4 Methaphosphoric acid/HPLC (Kurilich et al., 1999)
76 (Pfendt et al., 2003)
127.7–129.3 (Podsedek et al., 2006)
87–109 No available (Davey et al., 2000)
Cauliflower (Brassica oleracea
var. botrytis)
48.2 Total ascorbic acid (USDA, 2010)
81 Trichloroacetic acid/HPLC (Puupponen-Pimi¨
a et al., 2003)
40.6–52.4 Till-mans method (Sikora et al., 2008)
50 Metaphosphoric acid/2,6-dichlorophenol (Bahorun et al., 2004)
17.2 HCl/2,6-dichlorophenol (Pfendt et al., 2003)
64 Citric acid/HPLC-UV (Hrncirik et al., 2001)
54.0 63.1 Methaphosphoric acid/HPLC (Vanderslice et al., 1990)
42.0 (Kurilich et al., 1999)
64–78 No available (Davey et al., 2000)
Chinese broccoli (Kai lan)
(Brassica alboglabra)
28.2 Total ascorbic acid (USDA, 2010)
Chinese cabbage (Pak choi)
(Brassica rapa var. chinesis)
45.0 Total ascorbic acid (USDA, 2010)
25.3 Metaphosphoric
acid/2,6-dichlorophenol-indophenol
(Bahorun et al., 2004)
29 Methaphosphoric acid/HPLC (Wills et al., 1984)
Chinese cabbage (Pe tsai) (Brassica
rapa var. pekinensis)
27.0 Total ascorbic acid (USDA, 2010)
11 Citric acid/HPLC-UV (Hrncirik et al., 2001)
20 Methaphosphoric acid/HPLC (Wills et al., 1984)
(Continued on next page)
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1080 R. DOM´
INGUEZ-PERLES ET AL.
Tab l e 1 Content in vitamin C (mg 100 g1fw) of fresh edible parts of Brassica plants (Continued)
Commodity AA Vitamin C Extraction/analysis method Source (Reference)
Chinese flowering cabbage (Choi
sum) (Brassica rapa var.
parachinensis)
46 Methaphosphoric acid/HPLC (Wills et al., 1984)
Collards (Brassica oleracea var.
viridis)
35.3 Total ascorbic acid (USDA, 2010)
92.7 93.3 Methaphosphoric acid/HPLC (Vanderslice et al., 1990)
Curly kale (Brassica oleracea var.
acephala)
120 Total ascorbic acid (USDA, 2010)
107 Till-mans method (Sikora et al., 2008)
51.3 Methaphosphoric
acid/dinitrophenylhydrazine method
(Fonseca et al., 2005)
92.6 HCl/2,6-dichlorophenol-indophenol (Pfendt et al., 2003)
55.52 Methaphosphoric acid/HPLC-UV (Mart´
ınez et al., 2009)
730969(Hagen et al., 2009)
186 Not available (Davey et al., 2000)
Mustard cabbage (Indian mustard)
(Brassica juncea var. juncea)
70.0 Total ascorbic acid (USDA, 2010)
36.2 36.2 Methaphosphoric acid/HPLC (Vanderslice et al., 1990)
100 (Wills et al., 1984)
Mustard spinach (Tender greens)
(Brassica rapa var. perviridis)
130.0 Total ascorbic acid (USDA, 2010)
Red cabbage (Brassica oleracea var.
capitata)
57.0 Total ascorbic acid (USDA, 2010)
62.0–72.5 Methaphosphoric acid/HPLC-UV (Podsedek et al., 2006)
Savoy cabbage (Brassica oleracea
var. capitata)
31.0 Total ascorbic acid (USDA, 2010)
49.8–65.7 Methaphosphoric acid/HPLC-UV (Podsedek et al., 2006)
33.3 (Mart´
ınez et al., 2009)
White cabbage (Brassica oleracea
var. capitata)
36.6 Total ascorbic acid (USDA, 2010)
5.5 25.6 Manufactured kit/HPLC (G¨
okmen et al., 2000)
44 Citric acid/HPLC-UV (Hrncirik et al., 2001)
28.2 HCl/2,6-dichlorophenol (Pfendt et al., 2003)
18.8 Metaphosphoric
acid/2,6-dichlorophenol-indophenol
(Bahorun et al., 2004)
18.0–35.6 Methaphosphoric acid/HPLC (Podsedek et al., 2006)
42.3–67.0 44.3–74 Not available (Vanderslice et al., 1990)
17.0–24.0 (Kurilich et al., 1999)
46–47 (Davey et al., 2000)
32 (Chu et al., 2002)
43 (Puupponen-Pimi¨
a et al., 2003)
34.1 (Mart´
ınez et al., 2009)
White or yellow mustard (Brassica
alba)
3 Total ascorbic acid (USDA, 2010)
Turnip tops (Brassica rapa var.
Rapiferaa)
21.0 Total ascorbic acid (USDA, 2010)
46 MeOH:H2O/HPLC (Francisco et al., 2010)
89.39 Methaphosphoric acid/HPLC (Mart´
ınez et al., 2009)
Turnip greens (Brassica rapa var.
Rapa)
60.0 (USDA, 2010)
62 MeOH:H2O/HPLC (Francisco et al., 2010)
67.5 Methaphosphoric acid/HPLC (Mart´
ınez et al., 2009)
70 Not available (Mondrag´
on-Portocarrero et al., 2006)
NDB =USDA nutrient databank identifier, mg g1dw; ∗∗mg Kg1pf.
increase was observed in leaves and stalks in adult plants. In-
deed, Brassica byproducts (harvest remains) are foodstuffs rich
in health-promoting nutrients including vitamins and minerals,
with even higher values that those found in marketable heads
(Omary et al., 2003; Mart´
ınez et al., 2009; Dom´
ınguez-Perles
et al., 2010). Consequently, the stage of plant development con-
ditions the content of phytochemicals including vitamin C.
2.3. Environmental Factors
Concerning “external” environmental and agronomic fac-
tors that influence the vitamin C contents of Brassica crops
(Howard et al., 1999), sun light, aerial temperature, and soil
salinity have been highlighted as critical factors for vitamin C,
and therefore modifiers of the nutritional quality of Brassicas
(Lee and Kader, 2000; Moreno et al., 2007a; L´
opez-Berenguer
et al., 2009; Dom ˜
Anguez-Perles et al., 2010). With regard to
sunlight, although vitamin C synthesis in plants is not directly
depending on light, AA is synthesized from glucose obtained
through the photosynthesis, which let to an indirect relation-
ship between both, amount and intensity of sunlight and the
vitamin C content (Lee and Kader, 2000). In the same way,
Perez-Balibrea et al. recorded higher contents of vitamin C in
broccoli sprouts grown under a 16/8 h light/dark cycle, that
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BRASSICA FOODS AS A DIETARY SOURCE OF VITAMIN C 1081
significantly surpassed those of the sprouts grown in the dark,
by 83% on average (P´
erez-Balibrea et al., 2008). Likewise, the
relationship between air temperature and AA content has also
been reported for Brassica vegetables and, in general, growing
under low temperature regimes has as consequence a higher
vitamin C contents in plants (Lee and Kader, 2000).
Considering abiotic stress such as salinity in the irrigation
water, its concentration is crucial for the vitamin C content
of edible parts of Brassicas, including broccoli, decreasing pro-
portionally to the water physiological deficiency or hydric stress
(Toivonen et al., 1994). Several production areas of semiarid cli-
mates worldwide are affected by water shortage, and character-
ized by high-salt concentrations in the available irrigation water,
which has been pointed out as responsible of the variations in the
nutritional value of Brassica foods. However, the variation in vi-
tamin C content, as a consequence of the irrigation using saline
water, is closely related to the organ considered: while broccoli
inflorescences and stalks were not affected, the broccoli leaves
showed a decrease (15% as average) in vitamin C at 100 mM
NaCl (L´
opez-Berenguer et al., 2009; Dom ˜
Anguez-Perles et al.,
2010).
Fertilization practices are also critical for growth and the nu-
tritive composition of crops, and the effects on the vitamin C
of Brassica plants depends on type of nutrient and the applied
dose. The sulfur fertilization (60–200 Kg Ha1)atlowortoo
high rate at different flowering moments resulted in distinct vita-
min C contents with a positive effect of rich sulfur fertilization,
at the beginning of the inflorescence development, undergoing
a progressive reduction in concentration during heads forma-
tion (Vallejo et al., 2003a, 2003b). For nitrogen, its application
(100–400 Kg Ha1) severally leads to higher vitamin C concen-
trations in vegetables (Stefanelli et al., 2010), and among Brassi-
cas, cauliflower and white cabbage have displayed an increased
vitamin C content when the nitrogen based fertilization was
at low rates (Sorensen, 1984; Lisiewska and Kmiecik, 1996).
However, it has not been registered significant differences for
vitamin C content of broccoli, suggesting the relative effect of
fertilization practices on its content, as well as the contribution
of climate and water status together with the fertilization effects
(Sorensen, 1984; Lisiewska et al., 2008; Stefanelli et al., 2010).
The AA appeared to be strongly affected by a fast oxidation
to DHA under nonadequate growth conditions for broccoli. In-
deed, both seasonal and annual variations of the AA and total
vitamin C have also been observed (between 13.37–110.30 and
57.35–131.35 mg/100 g fw, respectively), for example, in broc-
coli harvested in separated seasons for two consecutive years
(Koh et al., 2009).
Harvesting marks the limit between pre- and postharvest.
Manipulations at harvest may cause damages on the integrity of
Brassica tissues as a result of bruising, surface abrasions, and
cuts. Consequently, harvesting methods may have pernicious
effects on vitamin C content, accelerating its loss or degrada-
tion by exposing it to external oxidative atmospheres. Like this,
the method employed for harvesting, either by hand or using
machinery, can determine the severity of the damages caused to
the marketable products. Therefore, harvesting procedures and
practices should be the less damaging as possible to avoid vita-
min C losses and keep the integrity of the item and its content
and, in addition, must be stored at low temperatures (Lee and
Kader, 2000; Sikora et al., 2008).
3. POSTHARVEST CONDITIONS AFFECTING
VITAMIN C CONTENT IN BRASSICA PRODUCTS
Post-harvest products would determine the potential amount
of nutrients and health promoting bioactives for dietary intake by
final consumers and, hence, their properties for consumers well-
being. The food composition would be greatly influenced by the
processes at this stage. Once harvested, the biological processes
that continue in food, are closely linked to the variation of phy-
tochemical composition during handling and storage. Because
of this, preserving the phytochemicals in Brassica vegetables
through careful post-harvest practices means to guarantee their
high nutritional quality and safety (Allende et al., 2006).
In this sense, vitamin C has been considered a bio-indicator of
adequate handling and processing procedures because of its sen-
sitivity to degradation (it is easily oxidized by both enzymatic
and nonenzymatic pathways) (Morrison, 1974; Clegg et al.,
1976) and, in general, fresh Brassica foods contain higher vi-
tamin C contents than stored foods, not only as a result of the
slight increase of vitamin C occurred in some species during
first days after harvesting (Eheart and Odland, 1972; Wu et al.,
1992), but also because it is not possible to stop the degra-
dation processes after harvest. Vitamin C losses begin during
pre-market preparations of Brassica vegetables, which may in-
clude bruising, trimming, and cutting, which can display an in-
tense reduction as a result of these processes that entails a weak
commercial and healthy value (Lee and Kader, 2000; Sikora
et al., 2008). Moreover, there are a broad array of post-harvest
factors affecting vitamin C content of Brassica vegetables such
as storage temperature, packing atmospheres, edible coatings,
and cooking methods. In fact, the combination of all these factors
will notably affect the final vitamin C content of foods-as-eaten,
as it has already been noted for some Brassica vegetables in-
cluding Broccoli (Puupponen-Pimi¨
a et al., 2003; Lemoine et al.,
2007; L´
opez-Berenguer et al., 2007), collards (Vanderslice et al.,
1990), cabbage (Kader; Vanderslice et al., 1990; Puupponen-
Pimi¨
a et al., 2003), mustard greens (Vanderslice et al., 1990),
and cauliflower (Puupponen-Pimi¨
a et al., 2003). These reports
have showed that the chain of factors from the producer to the
consumer let to degradation of vitamin C to different extends
for Brassicas.
3.1. Storage Temperature
This factor is critical for the maintenance of the vitamin C
level in Brassica spp. foods (Table 2). Refrigeration of Brassica
derived foods is used to maintain the vitamin C concentration
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1082 R. DOM´
INGUEZ-PERLES ET AL.
Tab l e 2 Content in vitamin C (mg 100 g1fw) of stored and cooked edible parts of Brassica plants
Commodity Frozen Refrigerated Cooked (cooking method) Source (reference)
Broccoli 40.1 (USDA, 2010)
56.0 (frozen); 23.1 (boiled/frozen) 106–134 40.1 (boiled); 116.2 (microwaved) (Vanderslice et al., 1990)
56.4 71.7–62.2/2 (Mangels et al., 1993)
64.3–73.7 (Favell, 1998)
77–89 (frozen); 77–86
(blanched/frozen); 69–80
(microwaved/frozen)
115–116 90-135 (blanched); 112–117
(microwaved)
(Howard et al., 1999)
84 (pillow packed) (Hussein et al., 2000)
55–56 (florets blanched/frozen);
35–36 (stems blanched/frozen)
(Murcia et al., 2000)
(Murcia et al., 2000)
90 (boiled) (Davey et al., 2000)
73 (boiled); 75 (high pressure
boiled); 106 (steamed); 54.9
(microwaved)
(Vallejo et al., 2002a)
18–21 (Franke et al., 2004)
35.2–83.5 (floret boiled);
36.0–100.0 (stem boiled);
35.5–85.1 (floret microwaved);
36.5–103 (leaves microwaved)
(Zhang and Hamauzu, 2004)
110–170 (L´
opez-Berenguer et al., 2007)
65–120 (stir fried) (Moreno et al., 2007b)
20 (frozen) 60 (blanched); 25 (boiled) (Sikora et al., 2008)
62.7 (frozen); 373.2
(blanched/frozen)
(Patras et al., 2011)
40 (CMC coated); 52 (chitosan
coated)
(Ansorena et al., 2011)
Brussels sprouts 74.1 62.0 (USDA, 2010)
30-50 (frozen) 15-40 (boiled); 35-80
(blanched)
(Sikora et al., 2008)
Cauliflower 55 (Davey et al., 2000)
66–73 14.4 (boiled); 73 (Blanched) (Puupponen-Pimi¨
a et al., 2003)
35 35 (blanching); 25 (boiled) (Sikora et al., 2008)
Chinese cabbage
(Pak-choi)
26.0 (USDA, 2010)
14–15 (Franke et al., 2004)
Chinese cabbage
(Pe-tsai)
15.8 (USDA, 2010)
68–10 (Franke et al., 2004)
Collards 18.2 (USDA, 2010)
41 (boiled) (Vanderslice et al., 1990)
Curly Kale (USDA, 2010)
62 (Davey et al., 2000)
45 15 (boiling); 65 (blanching) (Sikora et al., 2008)
465-828(Hagen et al., 2009)
Mustard cabbage
(Indian mustard)
25.3 (USDA, 2010)
4.8 (boiled) (Vanderslice et al., 1990)
Mustard spinach
(tender greens)
65.0 (USDA, 2010)
Red cabbage 10.8 (USDA, 2010)
Savoy cabbage 17.0 (USDA, 2010)
White cabbage 37.5 (USDA, 2010)
24.4 (boiled) (Vanderslice et al., 1990)
Turnip tops 26.8 18.2 (USDA, 2010)
29.4 (steamed); 0 (boiled/high
pressure boiled)
(Francisco et al., 2010)
Turnip greens 4.4 3.9 (USDA, 2010)
20–30 (frozen); 25–35 (dried,
blanched, frozen)
(Mondrag´
on-Portocarrero et al.,
2006)
39.7 (steamed); 0 (boiled/high
pressure boiled)
(Francisco et al., 2010)
NDB =USDA nutrient databank identifier.
mg 100g1dw.
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BRASSICA FOODS AS A DIETARY SOURCE OF VITAMIN C 1083
and temperature regimes <4C guaranteed a minor decrease,
whereas higher temperatures entailed significant reductions
(Ezell and Wilcox, 1959). It is generally accepted that storage,
at controlled low-temperatures, reduces the degradation of vita-
min C, but the Brassica species considered, the storage period,
and the fluctuations of temperatures may also act as modulators
for this vitamin losses (Adisa, 1986). In this aspect, for exam-
ple; the content in vitamin C of kale and cabbage underwent
an accelerated reduction stored at temperatures higher than 8C
(Ezell and Wilcox, 1959).
3.2. Duration of Storage
Differences between short and long-time periods of stor-
age are critical for the vitamin C content. Among the separate
Brassica products depending on the specie considered (roots,
leaves, or inflorescences), short-time storage at temperatures
below 8C allowed a quite stable concentration of vitamin C
(Ezell and Wilcox, 1959; Wu et al., 1992). However, for long-
time storage (3–6 weeks) at 1–2C, the fall of vitamin C contents
was dependent on the species. Thus, these losses varied from
5–10%, for broccoli, Brussels sprouts, and Chinese cabbage, to
a much severe reduction of more than 50% for kale (Albrecht
et al., 1990; Klieber and Franklin, 2000; Hagen et al., 2009).
In addition to the decrease of vitamin C under long-time re-
frigerated storage, an increase in the proportion of DHAA with
respect to AA has been described owed to the degradation of
AA, rendering DHAA (Wills et al., 1984; Lee and Kader, 2000;
Hagen et al., 2009). In spite of this, the reported losses of AA
in cruciferous vegetables are minimal in comparison to other
horticultural products, due to the high contents of these plants
in glutathione and other sulfur molecules involved in the reduc-
tion of DHAA to AA that, hence, allows a higher capacity for
AA retention during storage that reach between 65% and 95%
of initial levels, depending on the considered specie (Albrecht
et al., 1990; Lee and Kader, 2000).
3.3. Physical Pretreatments
Together with the low temperature-based storage, other phys-
ical treatments can help to preserve the nutritive value of Bras-
sica vegetables stored for long periods. In this way, it has been
reported the beneficial effects of hot air or ultraviolet light treat-
ments (UV-C) on minimally processed broccoli florets prior
to refrigeration, allowing a smaller decrease of both AA and
DHAA in treated broccoli than in controls (Lemoine et al.,
2007; Lemoine et al., 2010). On the other hand, Ansorena et al.
recently described that broccoli inflorescences treated with edi-
ble coatings presented even two times higher AA retention than
those uncoated. Among different coating tested, chitosan dis-
played the best performance and, next to other advantageous
impacts on broccoli quality, this effect was enhanced when it
was combined with a mild heat-shock, constituting a promis-
ing technique for Brassica manufacturing industry (Ansorena
et al.).
3.4. Freezing
The storage of Brassica vegetables at 30C for long pe-
riods (12 months) resulted in reduced vitamin C contents, in
the range of 15–18% for broccoli, 6–13% for cauliflower, and
32% for cabbage (Lisiewska and Kmiecik, 1996; Puupponen-
Pimi¨
a et al., 2003). The main cause of vitamin C reduction in
frozen Brassica foods has been the effect of the freezing pro-
cess in the internal structure of the vegetables. Differences in
vitamin C concentrations between fresh and frozen cauliflower
and cabbage were recorded, and varied from 16–30%, respec-
tively (Puupponen-Pimi¨
a et al., 2003). Contrary to this, contro-
versial results have been shown for fresh and frozen broccoli
inflorescences. While some authors indicated an important de-
crease (about 50%) as consequence of freezing (Lisiewska and
Kmiecik, 1996; Murcia et al., 2000), other reports remark the
protective effect of blanching on the vitamin C losses. In this
way, broccoli heads blanched prior to freezing underwent a re-
duction of the vitamin C losses of 83% (Patras et al., 2011).
In fact, blanching, far of being considered harmful, protects
vitamin C from degradation. Nonetheless, blanching also re-
duces the content of vitamin C, mainly because of denatura-
tion by heat and diffusion to the blanch-hot water (Vanderslice
et al., 1990), but the decreases produced by the further freezing
are minimal for kale, broccoli, cauliflower, or Brussels sprouts
in comparison with that observed in vegetable directly frozen
(Sikora et al., 2008; Patras et al., 2011). The reason why vitamin
C preservation, in blanched Brassica foods is less affected by
frozen-storage than those nonblanched, was suggested as result
of the effect on denaturation of catabolic enzymes present in
fresh vegetables (Howard et al., 1999; Lee and Kader, 2000;
Sikora et al., 2008; Patras et al., 2011). Consequently, the com-
bination of distinct temperature-based preservative procedures,
blanching, and freezing, enables the reduction of vitamin C
losses when freezing is used and, thus, help to guarantee high
vitamin C contents in frozen Brassica foodstuffs.
3.5. Controlled or Modified Atmospheres of Packing
The technological approaches to reduce the vitamin C losses
of Brassica vegetables during storage, include the use of low
partial pressures of O2and high partial pressures of CO2,inor-
der to decrease the metabolic activity of plant tissues to avoid the
degradation of the marketable and nutritional quality (Kader).
Brassica species showed different tolerance to modified atmo-
sphere packing (MAP), mainly because of the distinct resis-
tance of the edible organ used or processed (inflorescences, baby
leaves, leaves, stems, bulbs, roots, etc.), the physiological state
at harvest, and the concomitant storage factors (temperature,
humidity, and duration) (Ahvenainen et al., 1998; Mart´
ınez-
S´
anchez et al., 2006). Therefore, modified or controlled atmo-
sphere for Brassica products must be specifically designed. Nev-
ertheless, promising approaches have been performed indicating
not only that a retention of vitamin C, as in kale or turnip tops, is
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1084 R. DOM´
INGUEZ-PERLES ET AL.
possible, but also an increase during storage as found in broccoli
(Fonseca et al., 2005; Wold et al., 2007; Cefola et al., 2010).
Additionally to the use of MAP, the conditioning of broccoli in-
florescences with cytokinin (50 ppm of benzyl adenine), a plant
hormone with antioxidant properties involved in the delay of
the senescence and the decrease of the sensitivity to ethylene
(Chang et al., 2003), helped to reduce the fermentation of pack-
aged broccoli heads, preventing the degradation of vitamin C
(Khalili et al., 2008).
3.6. Domestic Cooking
Prior to consumption, every cooking method affects vitamin
C differently and has critical consequences on the protective
intake of vitamin C from Brassica vegetables. Likewise, while
microwave cooking method reduces the content in vitamin C of
broccoli from 20% to 40% as compared to raw broccoli (Vallejo
et al., 2002a; L´
opez-Berenguer et al., 2007), boiling, which
is the most classical domestic cooking for Brassicas, reduces
vitamin C almost two times more than the microwave, probably
due to the release of vitamin C into the cooking water (L´
opez-
Berenguer et al., 2007; Sikora et al., 2008). Actually, boiling
has been reported to induce a great decrease in vitamin C levels
of the Brassicas, these losses have been quantified in 24% and
80% for green cauliflower and kale, respectively. Moreover,
boiled-frozen vegetables showed even higher losses, owed to the
lack of structural integrity, than occurred when freezing without
previous treatments (Sikora et al., 2008). Relating to the effect
of stir-frying on vitamin C content of broccoli, Moreno et al.
showed the critical relevance of the kind of edible oil used for
cooking on the reduction of vitamin C contents. The decreases
registered reached the 8 and 81% for extra virgin olive oil and
refined olive oil, respectively. (Moreno et al., 2007b). Steaming,
by the contrary, has been shown as the thermal cooking process
that causes the lowest vitamin C loss in Brassica foods (Vallejo
et al., 2002a; Volden et al., 2009; Francisco et al., 2010).
The cooking time is also relevant, because of the exposition
time to the high temperatures during cooking as well as the long
time between preparation and consumption, that are all factors
that reduces the vitamin C, should be reduced to the minimum
(Lee and Kader, 2000; Campos et al., 2009).
As seen in this section, a broad array of postharvest fac-
tors affects the vitamin C of Brassica vegetables are not fully
addressed. Regardless the many studies that have been carried
out focused in either only one or a few processes or factors, not
enough multifactorial, integrative, and translational research has
been taken, in order to clarify how handling, storage, and final
consumer operations modify the vitamin C content of the healthy
horticultural products. Therefore, aiming to offer the highest
and most complete health-promoting phytochemical composi-
tion of foods, both the implementation of the most consecutive
postharvest practices and the communication to consumers of
the best guidelines for the proper processing of Brassica food-
stuffs should be encouraged.
4. BIOAVAILABILITY, METABOLISM, AND
EXCRETION OF DIETARY VITAMIN C
Vitamin C is an essential nutrient involved in the cell physi-
ology and several crucial processes for human health. Because
of evolutive selection has produced the lack of the enzyme that
catalyze the last step for AA synthesis, L-gulonolactone oxidase
(GulL-ox), humans are unable to synthesize it and, thus, vitamin
C has to be incorporated in through its dietary intake (Nishikimi
et al., 1994).
This essential nutrient is generally available from fruits and
vegetables as it has been aforementioned; Brassicas are a good
rich source of vitamin C. Despite its elevated content in these
vegetables, differences concerning the absorption of vitamin C
from Brassicas could be due not only to the content in the final
product, but also to the simultaneous presence of other interfer-
ing compounds as phenolics. In addition, different sources of
vitamin C may entail variations in its gastrointestinal absorp-
tion and, thus, affecting its bioavailability and physiological
effects (Mangels et al., 1993; Park and Levine, 2000; Song
et al., 2002). The comparative analysis of the bioavailability
of vitamin C from different dietary sources including Brassica
spp., Citrus spp., and pure compound (synthetic AA) did not
show relevant differences among foods, except for raw broc-
coli (Mangels et al., 1993). Interestingly, distinct foods (mainly
Citrus spp.) and cooked broccoli displayed similar vitamin C
bioavailability, higher than the registered after the raw broccoli
intake. This fact has been attributed to both the distinct release of
vitamin C in the intestinal lumen and its availability for organic
uptake as affected by the food matrix. Consequently, the work
of Van Het Hof et al. suggests that the consumption of Brassi-
cas, exposed to thermal or domestic processing, are better than
eating raw foods in terms of vitamin C intake, and could yield
a higher, albeit not so significant, bioavailable vitamin C (Van
Het Hof et al., 1999).
4.1. Bioavailability and Metabolism of Vitamin C: Focus on
the Role of other Brassica Phytochemicals
Vitamin C, both in reduced (AA) and oxidized form (DHAA),
undergoes several steps from the initial ingestion through its
elimination out of the human body. Initially, the uptake occurs,
for both AA and DHAA, in the epithelial cells of the small
intestine but in different physical locations, and different trans-
porters based in substrate-saturable mechanisms are used for
both forms (Li and Schellhorn, 2007a).
The efficiency in the absorption constitutes an essential factor
conditioning the further bioavailability of vitamin C. The AA
uptake constitutes the major source of vitamin C supply, as the
efficiency of its uptake is higher than for the DHAA, because of
the high affinity of AA for its receptor, contrary to the DHAA
(Malo and Wilson, 2000). The AA is absorbed through a sodium-
dependent vitamin C transporter type I (SVCT1) located in the
apical brush-border of the ileum (Malo and Wilson, 2000; Mart´
ı
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BRASSICA FOODS AS A DIETARY SOURCE OF VITAMIN C 1085
et al., 2009), and also through a sodium-dependent vitamin C
transporter type II (SVCT2), found in cells of most other tissues,
suggesting its implication in the transport to the intracellular
compartment.
On the other hand, cellular uptake of DHAA is performed by
ubiquitous glucose transporters of the GLUT family in duode-
num and jejunum (Deutsch, 2000) and, hence, as a likely con-
sequence of sharing the same transporters, changes in glucose
serum levels, characteristic of same metabolic diseases cours-
ing with glycemic deviation as diabetes, may reduce the DHAA
bioavailability (Agus et al., 1997; Rumsey et al., 1997). Fur-
thermore, regardless that the AA and the glucose are absorbed
in distinct segments of the small intestine and through different
transporters, glucose also could interfere with AA uptake since
ascorbate transport depends on an electrogenic process modu-
lated by glucose (Malo and Wilson, 2000). Therefore, glucose
content of foods and glycemic state of the subject also may mod-
ify the total vitamin C bioavailability, which must be taken into
account in order to guarantee the accurate vitamin C nutritional
status upon the variations in dietary habits.
Other factors altering the vitamin C absorption are the phe-
nolic compounds present in Brassica, secondary metabolites
with health-promoting effects that modify metabolic processes
(Vallejo et al., 2002b; Williams et al., 2004; Moreno et al., 2006;
Velasco et al., 2011). In fact, antagonistic effects on AA uptake
have been exhibited by different flavonoids including flavanols,
flavones, and isoflavones through the inhibition of SVCT1 (J.
B. Park and Levine, 2000; Song et al., 2002). On the other
hand, flavonoids and phenolic acids have also been considered
as blockers of intestinal glucose transporter isoform 2 (GLUT2)
and, therefore, able to regulate the glucose transport (C. Park
et al., 1999; Song et al., 2002; Manzano and Williamson, 2010).
Hence, in relation to this effect on the glucose metabolism,
another indirect interaction between phenolics and vitamin C
might be established owing to the role of glucose in vitamin
C absorption. Nevertheless, further trials should be designed in
order to assess the effects of Brassica polyphenols on vitamin
C bioavailability.
Glucosinolates, the other group of compounds characteris-
tics of Brassica, and their cognate bioactives, isothiocyanates,
could also affect the dietary availability of vitamin C. To this
date, there no a report or communication linking both directly,
either glucosinolates or isothiocyanates, to AA or DHAA ab-
sorption. However, isothiocyanates have been suggested to alter
the behavior of glucose transporter GLUT4 in vitro, and thereby
varying the glucose transport (Goto et al., 1992; Sujatha et al.,
2010). Similarly, DHAA absorption could also be affected be-
cause of the shared uptake mechanism used by both DHAA
and glucose (Deutsch, 2000). Therefore, new studies should be
performed to investigate whether Brassica glucosinolates may
vary the bioavailability of the vitamin C contained in the food
matrix, presumably by modifying the glucose metabolism.
After absorption, vitamin C forms are transported to the cells
by blood vessels, and during this distribution to the tissues, they
must be protected from oxidative reactions, being its interaction
with metal ions such as copper, iron, molybdenum, or cobalt
the major risk factors for AA oxidation. In fact, to prevent
deleterious reactions, ions reactivity is controlled by specific
chaperones (Harrison et al., 2000).
Once inside the cells, AA acts as cofactor and electron donor
in a broad number of enzymatic and nonenzymatic processes
in all cellular compartments. These reactions yield ascorbate
free radical (AFR) (De Tullio and Arrigoni, 2004) that is pro-
cessed to DHAA into the endoplasmic reticule as the main
route by which AA is oxidized to DHAA (Arrigoni and De
Tullio, 2002). Later on, AFR may take part of other metabolic
processes intended for its reduction back to AA: by NADH-
dependent AFR-reductase in the endoplasmic reticule and mi-
tochondria (Green and O’Brien, 1973) and by NAD(P)H in an
electron transport system mediated by CoQ in the plasma mem-
brane (Villalba et al., 1995; G´
omez-D´
ıaz et al., 1997). Even
so, the human organism is able to recycle the oxidized AA
(DHAA) to the reduced form (AA), but this path is not enough
for supplying the metabolic requirements and, hence, additional
external contributions by dietary sources are necessary. Conse-
quently, Davey et al., 2000, proposed that increasing half-life
and efficiency of each ascorbate molecule by the increase of the
DHAA recycling from erythrocytes, through improving erythro-
cyte glutathione (GSH) levels, could be an strategy to enhance
AA bioavailability (Davey et al., 2000). In recent years, de-
spite a GSH rise has been asserted in both in vitro models and
humans trials after Brassica foods ingestion and phytochemical
supplementations (M. F. Chen et al., 1995; Wark et al., 2004;
Pappa et al., 2007; Emmert et al., 2010), other studies with
human subjects displayed controversial results (Nijhoff et al.,
1995; Riso et al., 2009). These differences could be due to the
glutathione-S-transferase (GST) genotypic polymorphisms and,
thus, it seems reasonable that Brassica foods can increase cellu-
lar levels of GSH and/or GST in certain human genotypes (Wark
et al., 2004). Therefore, vitamin C intake related to Brassica
consumption might improve the bioavailability of this essential
nutrient by reducing the DHAA, owing to an augment of GSH
levels. Nevertheless, this hypothesis should be carefully evalu-
ated since it is currently believed that AA recycling is addressed
to limit DHAA formation as a tool to prevent deleterious or
toxic effect of DHAA, prior to being an efficient tool to provide
AA requirements. In fact, pernicious effects of DHAA on cells
have been reported when high levels are available, leading to
mitochondria damage (Martensson and Meister, 1991; Arrigoni
and De Tullio, 2002). But, interestingly, severe damage is only
presented under both GSH and ascorbate deficit (Martensson
and Meister, 1991), which constitutes an easily reversible status
through Brassica supplementation thanks to the high vitamin C
content in Brassica products as well as to the ability of Brassica
phytochemicals to increase the GSH levels (Chen et al., 1995;
Wark et al., 2004; Pappa et al., 2007; Emmert et al., 2010; Pen-
nington and Fisher, 2010). Hence, the likely improved reduction
of physiological DHAA after Brassica consumption, far from
being pernicious, might entail an improved bioavailability of
vitamin C.
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1086 R. DOM´
INGUEZ-PERLES ET AL.
Finally, for the urinary excretion of vitamin C, the circulating
AA is filtered in kidneys and part of the primary AA excreted is
further reabsorbed into the capillary bed surrounding the proxi-
mal convoluted tubules (Nelson et al., 1978). The physiological
machinery (digestive, circulatory, and renal systems) works to-
gether guarantying the supply of essential vitamin C. In this way,
when the intake of foods rich in vitamin C is low, the majority of
the vitamin contained in the food matrix is rapidly absorbed into
the small intestine and reabsorbed into the kidneys. However,
when high concentrations of vitamin C are ingested, the effi-
ciency of the absorption and reabsorption is modulated, turning
to a “less-efficient mechanism” in order to guarantee the opti-
mum vitamin C serum level (60–100 μmol L1) for the normal
development of physiological functions, avoiding the pernicious
effect of its excess (Levine et al., 1996).
4.2. Human Requirements for Vitamin C
Physiological stage, health condition, age, sedentary habits,
smoking, etc., are a plethora of factors that determine the neces-
sary dietary intake of vitamin C. The physiological mean con-
centration of vitamin C has been established in 20 mg Kg1of
body weight in well nourished humans being, whereas saturation
level is reached at 33 mg Kg1. Likewise, vitamin C disappears
of the organism at a rate of 3% per day, appearing deficiency-
related symptoms when levels fall below 7 mg Kg1during de-
pletion of vitamin C-rich foods (Blanchard, 1991; FAO, 2004).
Considering both absorption efficiency and catabolic rate of vi-
tamin C, the dose of 10 mg per day constitutes the minimal
supply for guarantying the physiological necessities, or to re-
vert any pathological sign linked to its deficiency. Consequently,
vitamin C recommended dietary allowance (RDA) was estab-
lished from 10 to 60 mg per day (Krebs-Smith and Clark, 1989).
Nevertheless, this recommended dose is currently under reeval-
uation because of available novel epidemiological data relating
vitamin C consumption to new physiological functions. There-
fore, the necessity of dietary intake ranges from 90 to 100 mg per
day to prevent cardiovascular diseases and cancer. Indeed, the
recommendation raised the level to 120 mg per day for prevent-
ing specific pathological conditions such as cataracts, although
this extremely high level needs to be experimentally supported
with further studies (Carr and Frei, 1999; FAO, 2004). Addition-
ally, other health disorders including diabetes, cachexia, drugs
dependence, and malabsorption syndrome may influence the
vitamin C requirements (Rebouche, 1991; Mart´
ı et al., 2009).
These health problems are connected to the vitamin C absorp-
tion and/or excessive ingestion and must be accounted for the
accurate determination of the daily needs of vitamin C.
Certain physiological conditions or developmental states also
require different vitamin C supplementation. For example, preg-
nancy and lactation are special physiological conditions with ex-
tra needs (as a result of a higher intensity of organic processes
as well as liquid retention and body mass differences) entailing
variations in vitamin C nutritional requirements. In this way,
while the RDA of vitamin is increased during pregnancy (by
16%) over the nonpregnant women, additional requirements for
dietary vitamin C are around 50–58% during lactation, to fulfill
both the mother and the infant needs, depending on the lac-
tation phase (Urgell et al., 1998). Likewise, during childhood,
the daily recommended intake for infants of 1–18 years of age
is 30–40 mg per day and it must be gradually increased un-
til reaching the necessities described for adulthood (Rees and
Shaw, 2007). Interestingly, regarding elderly, despite the fact
that the metabolic rate is decreased, higher doses are required
since vitamin C plasma concentration of this population group
is lower than in young adults, which has mainly been attributed
to disturbances in the intestinal and renal function (Heseker and
Schneider, 1994).
With respect to smoking, it has been suggested that smokers
need a 50% higher intake of vitamin C than nonsmokers to
ensure an optimal physiological concentration of AA able to
cope with the much higher oxidative reactions occurring in their
bodies as a consequence of this toxic habit (Kallner, 1987).
These general considerations on the vitamin C requirements
for distinct sub-population of humans are closely linked with the
dietary habits of the different collectives considered. In this way,
the requirements abovementioned convert the intake of fruits
and vegetables in a necessary source of vitamin C, among which
Brassicaceae is a highlighted vegetables family that guarantee
a healthy status in human populations, conferring additional
advantages (it constitutes a simultaneous source of fiber and
other essential vitamins and minerals) in comparison with the
use of synthetic forms on this nutrient. In addition, the extraction
of vitamin C from natural products reduces, and almost makes
it disappear, the risk of surpassing the upper limit.
This safe upper limit for vitamin C consumption has been
established in around 1 g per day as higher intakes have been re-
lated to pathological signs. Supplementation with 2–3 g per day
may cause diarrhea as a consequence of osmotic disturbances
of the unabsorbed vitamin C (Hathcock et al., 2005). Likewise,
it has also been described the oxalate-stone formation in kid-
neys when vitamin C is ingested in the range of 5–10 g per day,
although this has only been associated with high amounts of
urinary calcium (Urivetzky et al., 1992). Haemolysis has been
pointed out as triggered by toxic doses of vitamin C as well
(Delanghe et al., 2007). Moreover, chronic doses of 500 mg per
day or acute doses of 1–3 g may cause toxic effects expressed
as vasoreactivity, with relevant considerations on cardiovascular
and cerebrovascular diseases (Carr and Frei, 1999). However,
clinical findings linked to excessive intake of vitamin C are very
limited and linked to the administration of nutritional supple-
ments and not to vegetable foods (including Brassica or any
other natural foods).
5. THERAPEUTIC POTENTIAL OF DIETARY VITAMIN
C AND BRASSICA
Vitamin C has been pointed out as an essential nutrient with
an active role in the maintenance of body functions, displaying
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BRASSICA FOODS AS A DIETARY SOURCE OF VITAMIN C 1087
a wide range of therapeutic properties such as antioxidant, an-
ticarcinogenic, cofactor in the collagen synthesis, and promoter
of iron absorption (Hallberg et al., 1987; Franceschi et al., 1994;
Yoshikawa et al., 2001; Arrigoni and De Tullio, 2002; Telang
et al., 2007). In fact, a broad number of reports have been per-
formed in order to demonstrate the health-promoting properties
of vitamin C (Mart´
ı et al., 2009). Nevertheless, only a few works
have been focused on the role of dietary vitamin C on health,
even though the well-established effect of other nutrients and
the food matrix on the bioavailability of this vitamin is evident
as reviewed above. Regarding this, long periods with an insuffi-
cient intake of fresh vegetable foods can produce a reduction in
the serum levels of AA, with dramatic consequences, increasing
the formation of reactive oxygen species, leading to a greater
incidence of chronic diseases and aging (Benzie, 2003; Li and
Schellhorn, 2007b). Brassica foods have been related to the pre-
vention of degenerative diseases linked to oxidative processes
(Jahangir et al., 2009). In Brassicas, the 80% of their natural
antioxidant activity comes from phenolic compounds and vi-
tamin C, being vitamin C responsible of 10–12% of the total
antioxidant capacity of broccoli and cabbage (Podsedek, 2007).
In general, despite the complete range of reactions in which
vitamin C may be involved, as well as the sense of its contribu-
tion, that is not fully understood, its antioxidant properties, the
protection against free radicals, cytoprotective functions such
as prevention of DNA mutation, protection against lipid per-
oxidative damage, and repairing amino acid residues to save
the protein integrity have all been suggested (Hoey and Butler,
1984; Barja et al., 1994; Lutsenko et al., 2002). Moreover, the
consumption of Brassica foods as source of vitamin C has ad-
ditional advantages in comparison with other dietary sources of
vitamin C. In fact, joined to the rich-in-phytochemicals Brassica
food matrix, these health-promoting properties attributed to vi-
tamin C could be interestingly boosted. Actually, a wide range
of positive effects on some cardiovascular diseases has been
displayed by Brassicas in several assays (Kataya and Hamza,
2008; Akhlaghi and Bandy, 2010) and prospective studies. Kim
et al. has shown that the incorporation of dark green leafy cru-
ciferous foods to the diet can prevent coronary artery disease
in hypercholesterolemic men by decreasing risk factors (Kim
et al., 2008). In accordance to this, the regular supplementation
of kale juice reduces the intestinal lipid absorption, modulating
the lipid profile and thereby decreasing serum lipid substrates
available for peroxidation. So, the efficiency of the antioxidant
system was increased and, thus, the oxidative disturbances and
related conditions were eased (Kim et al., 2008).
Oxidative reactions are also in the basis of cancer initiation
and, hence, vitamin C may play an essential role in its pre-
vention (Lutsenko et al., 2002). Mechanism of action of AA
in the prevention of the deleterious activity of free radicals has
been connected to the generation of hydrogen peroxide (H2O2)
from O2and to the induction of apoptosis in cancer cells since
normal cells are significantly more resistant to H2O2than can-
cerous ones (Chen et al., 2005; Frei and Lawson, 2008). Healthy
levels of vitamin C in the organism can prevent DNA mutation
induced by oxidative stress as well (Lutsenko et al., 2002). Like-
wise, vitamin C has carried out functions related to cancer risk
reduction through diet, as it has been pointed out in epidemio-
logical trials, and the correlation between vitamin C intake and
cancer prevention has shown higher significance when consum-
ing fruits and vegetables as source of vitamin C instead of the
synthetic form (Dennison et al., 1998; Chen et al., 2005; Moreno
et al., 2006; Frei and Lawson, 2008). These contributive effects
have been also attributed to the role of other phytochemicals
with anticarcinogenic properties in Brassica (Tiku et al., 2008;
Jahangir et al., 2009; Kusznierewicz et al., 2010). In this sense,
glucosinolates, isothiocyanates, phenolic compounds, and vita-
min C may act synergistically in therapeutic functions. Clinical
trials supplementing single vitamins and minerals have indi-
cated the dependence or pharmacological benefits of vitamin
C owed to synergistic effects of food components in fruits and
vegetables (Blot et al., 1993; Loria et al., 2000; Bjelakovic et al.,
2007). Therefore, therapeutic features associated with Brassica
consumption are generated from the influence of multiple bioac-
tives acting in a cooperative action better than the sole biological
action of a single agent and more developments on this area are
expected.
As conclusive remarks, in spite of the many experimental
approaches existing so far, on the biological activity derived
of Brassica consumption, further comprehensive studies are re-
quired and should be conducted to ascertain the in vivo prospects
of such products, as the majority of the experimental procedures
have been carried out with in vitro models. Likewise, experimen-
tal animal and human interventions focused on the elucidation
of the multiple therapeutic properties of vitamin C in Brassica
vegetables and aiming to improve the real dimension of the
connections between food, nutrition, and health are needed.
ACKNOWLEDGMENTS
Authors would like to express their gratitude to the Spanish
Ministery of Science and Innovation (MICINN) for the funding
through the projects CICYT (AGL2007-61694). Part of this
work was also funded by the project “Group of excellence”
(04486/GERM/06) from the Regional Agency for Science and
Technology of Murcia (Fundaci´
on S´
eneca) and the Consolider-
Ingenio 2010 Fun-C-Food project (CSD2007-00063).
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... They are the most commonly grown vegetables worldwide because of their high contents of vitamins, carotenoids, tocopherol, minerals, folate, amino acids, carbohydrates, dietary fiber, and bioactive compounds, namely, glucosinolates and phenylpropanoids. They have commercial importance as components of the daily human diet and as a primary source for the vegetable oil industry [1][2][3]. ...
... The intake of these cruciferous vegetables plays a crucial role in antioxidation, improving the immune system, and preventing aging-related and cardiovascular diseases, as well as diabetes and cancers. These health benefits are related to antitoxic, anticancer, antioxidant, antidiabetic, and anti-inflammatory effects, and are mainly associated with the properties of secondary metabolites, including phenylpropanoids, carotenoids, vitamins, and glucosinolates, present in the Brassicaceae family [1][2][3][4][5]. ...
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... . As hortaliças deste grupo são excelentes fontes de nutrientes para população principalmente de sais minerais, antioxidantes como as vitaminas A, B, C e K, e carotenóides (Freire et al., 2003;Domínguez-Perles et al., 2014). ...
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... Broccoli, belonging to the cruciferous family, is an economically important vegetable crop that has been largely attributed to nutritional components such as minerals, vitamins, polyphenol, and a particularly high content of glucosinolates (GSLs) (Kmiecik et al. 2007;Dominguez-Perles et al. 2014;Mahn and Reyes 2012;Bhandari and Kwak 2015). GSLs are nitrogen-and sulfur-containing amino acid-derived secondary metabolites, which are mainly found in Brassica species, including broccoli (Brassica oleracea var. ...
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Broccoli, a Brassica crop, is an important vegetative crop because of its nutritional components and beneficial phytochemicals. Glucoraphanin (GR), a major glucosinolate (GSL) in broccoli, is converted by hydrolyzation of the endogenous enzyme, myrosinase, into sulforaphane (SR), which protects the body against a variety of chronic diseases. Despite their economic importance, biotechnological approaches for increasing GR content in Brassica species are still limited. The main objective of this study was to develop a GR-rich broccoli cultivar using the CRISPR/Cas9-mediated DNA-free genome-editing technique. It is considered that MYB28 is one of the key genes involved in the accumulation of GSL levels in broccoli. Furthermore, with increased GSL levels by introgression of MYB28 from wild species, B. villosa showed a 9 bp deletion in exon 3, leading to one amino acid substitution and the deletion of three amino acids. Therefore, we considered the 9 bp deletion to be the most significant change in GR-rich broccoli and conducted Cas9 protein and single-guide RNA transfection into broccoli protoplasts for editing the flanking sequence of the 9 bp deleted MYB28 gene. Finally, increased GR content was observed in broccoli regenerated from protoplasts with specifically edited MYB28.
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A Região Serrana do Estado do Rio de Janeiro (RSA-RJ) possui características edafoclimáticas favoráveis ao cultivo das mais variadas espécies de hortaliças e se localiza relativamente próxima a grande mercado da Região Metropolitana do Rio de Janeiro (IBGE, 2017; EMATER, 2020a, b). Dentre as diferentes hortaliças produzidas, merecem destaque as brássicas, assim chamadas por serem espécies pertencentes à família botânica Brassicaceae. Dentre as brássicas mais cultivadas e comercializadas nesta região estão as couves, da espécie Brassica oleracea, que são classificadas a nível infra específico em quatro variedades botânicas: couve-flor (B. oleracea var. botrytis), brócolis (B. oleracea var. italica), repolho (B. oleracea var. capitata) e couve-comum (B. oleracea var. acephala) (Melo et al., 2017). Estimativas apontam a colheita de mais de 105 mil toneladas de hortaliças do grupo das brássicas na RSA-RJ no ano de 2020, provendo um faturamento bruto de mais de 169 milhões de reais (EMATER-RJ, 2020a). Dentre os principais municípios produtores, destacam-se Nova Friburgo e Teresópolis com as maiores colaborações nesta produção (EMATER-RJ, 2020a, b; CEASA-RJ, 2021). Além da grande importância econômica, as brássicas têm grande importância social, para produtores e consumidores. O seu cultivo e comercialização são grandes geradores de empregos e de renda, com ênfase na agricultura familiar, uma vez que, o cultivo destas espécies está fortemente relacionado a este segmento (May et al., 2007; Santos, 2020). A produção de brássicas na RSA-RJ destina-se ao abastecimento do mercado local e, principalmente, da região metropolitana do Rio de Janeiro, além de parte da região Sudeste do Brasil. A RSA-RJ pode ser considerada uma parte importante do cinturão verde da capital e um importante polo econômico do Estado do Rio de Janeiro (CEASA-RJ, 2015; Bhering, 2017; Santos, 2020), sendo grande parte da produção comercializada nas Centrais de Abastecimento do Estado (CEASA-RJ). Diante do exposto, o presente trabalho tem como objetivo atualizar as informações, tendo como base as últimas pesquisas com culturas de brássicas, assim como relatar dados recentes sobre importância econômica e sistemas de produção adotados na Região Serrana do Estado do Rio de Janeiro.
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