Enhancing Iron Bioavailability of Vegetables through Proper Preparation-Principles and Applications

Enhancing Iron Bioavailability of Vegetables through Proper
Preparation?Principles and Applications
Ray-Yu Yang and Samson C. S. Tsou
AVRDC–The World Vegetable Center, Taiwan


ABSTRACT

Iron deficiency anemia is the most prevalent nutritional problem in the world today.
AVRDC? the World Vegetable Center, an international, non-profit organization, aims to
reduce malnutrition and poverty among the poor through vegetable research and
development. Iron bioavailability of vegetables and food preparation ways to increase
available iron in plants were investigated under the AVRDC Nutrition Program.
Principles derived from iron bioavailability studies have been applied to design
high-iron recipes based on conventional food preparations for iron-deficient areas,
including southern and northern India. Enhancing nutrient bioavailability through
optimum food preparations and legume-based recipe designs were effective in
increasing available iron intake of schoolchildren in India. High-iron recipes including
staple food and African indigenous vegetables based on East African countries are
presently under investigation. This paper summarizes the major findings of iron
bioavailability studies conducted mainly by the AVRDC and the applications of these
studies towards improving iron nutrition in developing countries through international
cooperation.
Key words: food-based nutrition, iron bioavailability, mungbean, recipes, tomato,
vegetables


J. International Cooperation 1 (1) (June 2006): 107-119
© 2006 International Cooperation and Development Fund

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108 June 2006
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Introduction
iron deficiency utilize supplements
and/or fortification of diets (Scrimshaw,
Iron deficiency is the most common
1996). An alternative and sustainable
nutritional disorder in the world and
approach would be to improve iron
affects more than one billion people,
bioavailability of plant-based diets.
particularly reproductive-age women and
pre-school children in tropical and
Food processing and iron chemistry
sub-tropical zones (ACC/SCN, 2000). It
are important factors affecting iron
also has a serious impact on school-age
bioavailability. The chemistry of iron,
children and working males. If uncorrected,
particularly its valence, solubility, and
iron deficiency leads to anemia of types of chelation, influence its absorption.
increasing severity, reduced work capacity,
Food processing methods, such as baking,
diminished learning ability, increased
canning, drying, and cooking can have
susceptibility to infection, and greater
different effects on iron bioavailability,
risk of death associated with pregnancy
and therefore should be considered.
and childbirth (ACC/SCN, 1998).
Current methods for estimating iron
bioavailability (IB) include animal
Iron deficiency results from diets
bioassays, human assays, cell models and
lacking in iron, reduced iron bioavail-
in vitro measurement. In vitro assay
ability, increased iron requirements due
involves simulated gastrointestinal digestion
to pregnancy, and losses due to parasitic
using a commercially available enzyme
infections. Absorption of plant-based iron,
and then measurement of the soluble iron
though variable, is considered lower than
released by this digestion to a dialysis
that of iron from meat and it is greatly
tubing. Thus, this in vitro iron
influenced by interactions with enhancers
bioavailability assay is called iron
and inhibitors (Layrissse et al., 1969;
dialyzability (ID) in this report. The in
Cook, 1983). Populations in developing
vitro measurement is simple, rapid, and
countries with limited resources avoid
inexpensive, and useful for food
hunger by consuming more plant-based
screening and identifying factors that
food than expensive animal based might influence iron availability.
products (Baker and Mayer, 1979; World
bank, 1994). The number of vegetarians
Vegetables provide multiple nutritional
is increasing worldwide, although their
functions to human diets. Some are rich
total iron intake may meet dietary in micro-nutrients particularly ?-carotene
recommendations (FAO/WHO, 1998), and iron; some provide macro-nutrients
iron deficiency is common among and energy (FIRDI/NPUST, 1998); while
vegetarians due to the low bioavailability
some are valued for health-promoting
of plant iron (Craig, 1994). Many factors (Harborne, Baxter and Moss,
nutrition programs aimed at decreasing
1999). In addition to their nutrient values,

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Yang and Tsou
Iron Bioavailability of Vegetables
109

vegetables nowadays are consumed AVRDC?Regional Center for Africa in
worldwide to provide attractions and
Tanzania, entitled “ Promotion of
diversification in diet (Willtee, 1994).
Neglected Indigenous Vegetable Crops
Higher consumption rate (vegetables and
for Nutritional Health in Eastern and
fruits, minimum 400 g and 5?9 servings a
Southern Africa” funded by Federal
day) is recommended for health mainten-
Ministry for Economic Cooperation and
ance and cancer prevention (Steinmetz,
Development (BMZ, Germany). In
1996; Law and Morris, 1998).
addition, this working model of the
Studies by Kapanidis and Lee (1995)
higher iron recipe design using African
at Rutgers State University, New Jersey,
indigenous crops is being planed to apply
had indicated that in vitro bioavailability
in West African regions to promote iron
of iron in cruciferous vegetables can be
consumption.
enhanced from 5% to more than 20%
The Principles
through cooking. On the basis of that
1. Cooking enhancing effect on ID of
study, experiments were designed by the
vegetables and fruits
AVRDC and collaborators to (1) survey
in vitro iron bioavailability of fruits and
1-1. ID of certain vegetables and fruits
vegetables in raw and cooked forms and
can be enhanced simply by boiling
investigate better iron-source vegetables;
in water (AVRDC, 1996 and 1997;
(2) better understand the principles and
Yang et al., 1998; Yang, Tsou and
mechanisms of cooking enhancing effects;
Lee, 2002): Plant commodities
(3) investigate household food prepar-
commonly consumed in Asian diets,
ation methods to increase available iron
including various types of 46
content in plant-based diets; (4) confirm
vegetables (leaf, fruit, root, stem,
through human study the enhancing
flower, legume and mushroom), 16
ability of vegetables as assayed by the in
fruits, and 2 cereals (rice and wheat)
vitro method; (5) design a legume-based
were measured for in vitro iron
diet with vegetables for higher iron
bioavailability in raw and cooked
consumption in South Asia.
forms. Boiling in water for 10 min
enhanced ID of 47 of the 64 of the
The legume-base diet with vegetables
tested commodities (Figure 1).
was proved effective in improvement of
nutrition status of school children. Higher
1-2. Vegetables can be categorized into
iron recipe designs with nutritional
three groups based on their ID of
studies of African indigenous vegetables
raw and cooked form (Yang, Tsou
and the previous iron bioavailability
and Lee, 2002): Based on the ID
studies are currently included in a
values of uncooked and cooked, the
center-wise project, managed by
46 vegetables and 2 cereals could be

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110 June 2006
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Wheat, whole

Rice, m illed

Eggplant

Celery
Cooked

Garland
Raw
Bas il

Lettuce

Indian bean

Cucum ber


Red leaves

Mus hroom

Kang-kong

Mungbean

Das heen

Mus tard leaves

Soy bean

Toothed

Rag gourd


Spinach

Onion

Veg. s oybean

Carrot

Coriander

Lotus

Radis h

Pea with pod

Bam boo s hoot


Paits ai

Spinach wo/ root

Wax-gourd

Lim a bean

Am aranth

Kidney bean

Bitter m elon

Sweet potato

As paragus


Leek flower

Onion fragrant

Borecole

Ginger

Corn, fres h

Pum pkin

Cabbage

Cauliflower

Pepper, red


Broccoli

Pepper, green

Tom ato

0%
5%
10%
15%
20%
25%
30%
35%
40%


Iron Dia lyzability (ID)

Figure 1. Iron Dialyzability (ID) of Raw and Cooked Vegetables

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Yang and Tsou
Iron Bioavailability of Vegetables
111

divided into three categories ?
from an average of 40.05 + 42.57 µg
Group 1: low ID in raw form but 2
to 75.03 + 53.37 µg per 100g of
times or more after cooking.
fresh weight. Boiling fruit produced
Seventeen vegetables fall in Group 1,
a similar result, from 32.29 + 25.06
including cabbage, broccoli, cauli-
µg/100 g to 43.54 + 23.82 µg/100 g.
flower, amaranth and green kidney
In general, cooked vegetables are a
beans. Group 2: Low ID in raw form,
better source of iron than fruits.
ID slightly improved by cooking. A
1-5. Boiling fresh vegetables provides
total of 24 items were in Group 2,
more available iron than process-
including carrot, celery, eggplant,
ing, including pickling, blanching,
dried beans, kang-kong, onion,
canning, and drying (AVRDC,
spinach, rice and wheat flour. Group
1996; Yang et al., 1998): Selected
3: Relatively high ID (>10 %) in raw
processed vegetable products were
and cooked forms. Bitter melon,
measured for ID and compared to
ginger, green and chili peppers,
that of fresh form. Canned tomato
sweet potato and tomato were in this
paste and canned whole tomato fruit
group 3.
show very low iron availability
1-3. Enhancing effect of cooking is not
compared to the fresh product. It
as apparent in fruit as in
might be due to lower bioavailability
vegetables (AVRDC, 1997; Yang et
of the extrinsic iron from the can
al., 1998): A wide variation in in
itself. Re-heated canned asparagus,
vitro iron bioavailability, ranging
bamboo shoots, and mushrooms
from 0.6 to 21%, was measured
could not increase ID. Pickling
among 16 selected fruits. An
might provide more acid soluble iron,
enhancing effect from cooking was
but no enhancing effect was
observed in half of the samples.
observed through further cooking.
Cantaloupe, grapefruit, kiwi, and
Cooking tofu did not affect ID of its
pineapple were found to have higher
raw form. Hot-air drying at 80oC
iron bioavailability compared to the
enhanced the iron bioavailability of
others tested.
raw cabbage, which has a cooking
1-4. Vegetables are a better iron source
effect, but did not enhance spinach,
than fruits (Yang and Tsou, 1998):
which has no cooking effect. Further
ID of vegetables, legumes and
cooking the dried sample did not
cereals ranged from 0.2% to 25.3%
affect ID. Therefore, pickling,
in raw form and 0.8% ? 33.8% in
canning, blanching, and hot-air
cooked items. Boiling vegetables in
drying can enhance ID of raw
water raised available iron content
materials. Double heating, like

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112 June 2006
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cooking samples which had been
1-8. ID of mungbean can be improved
blanched, hot-air dried, and canned
by sprouting or by adding vitamin
was not able to increase ID of these
C before cooking (AVRDC, 1995;
processed products. There is only
Yang et al., 1998): The iron
one enhancement in the first heat
content in seeds and sprouts was
treatment. Cooking the material
found to be similar, but higher
directly in boiling water for 10
vitamin C and lower phytic acid
minutes results in the most available
contents were observed during
iron.
mungbean sprouting process. Cooking
1-6. Enhancing effect of stir-frying is
slightly increased ID of mungbean
comparable to that of boiling
seeds, but greatly increased ID of
(Yang et al., 1998): Stir-frying with
sprouts. Addition of vitamin C (more
soybean oil is a common household
than 10-fold the iron content) could
cooking method for leafy vegetable
make iron in mungbean more available.
dishes in Asia, and it showed an
2. Enhancing effect on staple foods and
enhancing effect on tomato, cabbage,
iron dense food through cooking
spinach, and cauliflower, and was
with selected vegetables
found comparable to boiling. 2-1.Both raw and cooked tomato, and
Stir-frying is an alternative method
cooked cabbage and cauliflower
of preparation for vegetables, such as
exert an enhancing effect on an
spinach, which did not show an
iron-dense food such as laver
enhancing effect by boiling.
(Yang et al., 1998): The iron content
1-7. Cold storage suppresses ID of
of laver (Porphyra laciniata) is as
cooked vegetables (AVRDC, 1996):
high as 957 ppm. Mixtures of cooked
Storing raw tomato, spinach, and
cauliflower and laver produced more
cabbage overnight at 4oC did not
available iron than was produced
affect ID of uncooked form, nor did
when the samples were cooked
storing cooked samples for 3 hours
separately. This was also observed
at 4oC. Cold storage for more than
for cooing tomato and cabbage.
one day was found to reduce
Among these vegetables, tomato
available iron content of the cooked
produced the most pronounced
cabbage. This might be due to
enhancing effect. Addition of raw
vitamin C oxidation and the slow
tomato to cooked laver could
reduction of available iron through
increase available iron in the mixture.
interaction of the food matrix to
On the contrary, raw cabbage was
form a complex.
found to be an inhibitor in a mixture
of cooked laver and raw cabbage.

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Yang and Tsou
Iron Bioavailability of Vegetables
113

2-2. Available iron of cooked mungbean
ferritin, from which iron may be
is increased when mungbeans are
released by proteases or denaturation
cooked with tomato, cabbage and
by heat or low pH. Enzymes such
moringa (AVRDC, 1998 and 2000;
as polyphenol oxidases are
Yang et al., 1998): Legumes are
compartmentalized in cells until the
rich in protein. Often called “poor
cells are disrupted by blending or
man’s meat,” they constitute an
mastication. Almost immediately,
important supplement to the
the soluble iron becomes bound in
predominantly cereal-based diets in
iron-polyphenol complexes due to
Asia. In vegetarian diets, or in diets
the action of polyphenol oxidases,
containing low amounts of animal
and is thus rendered unavailable.
foods, they are an important source
Heating denatures the polyphenol
of protein. Mungbean was selected
oxidases preventing their action, but
as a basic ingredient and cooked
leaves intact a sufficient amount of
with other components to enhance
ascorbic acid to maintain iron in a
the ID of the mungbean-based diet.
soluble form through chelation, even
Cooking with cabbage or tomato and
at pH 2 in the stomach and pH 6-7 in
mixing with raw tomato helps
the intestine. Thus, more available
unlock the iron present in mungbean.
iron can be absorbed from cooked
Kale and sweet pepper showed no
cabbage than from the raw form.
such enhancing effect.
3-2. With/without and more/less iron
2-3. Cooking with tomato raises ID of
enhancers and inhibitors explains
soybean and lima bean (AVRDC,
the vegetable groups by cooking
2000): Tomato was tested with other
enhancing effect (AVRDC, 2000):
staple foods including sweet potato,
A strong iron chelator was used in
rice, wheat flour, soybean and lima
the cooking effect study to explain
bean. ID enhancement was observed
that (1) Group 1 vegetables such as
in soybean and lima bean when
broccoli, cabbage, and mustard
cooked with tomato.
leaves contained both enhancers and
heat related inhibitors. Cooking
3. Factors contributing to enhancing
eliminates the inhibitors, and then
effects on ID in cooked vegetables
enhancers raise up ID of cooked
3-1. Mechanism of the cooking
vegetables; (2) Group 2 vegetables
enhancing effect on cabbage
such as kang-kong, mungbean and
(AVRDC, 1999): A model was
soybean lack both heat related
proposed to explain how cooking
inhibitors and enhancers. Thus no
can enhance ID from cabbage ? Iron
cooking enhancing effect was
in plant cells is stored mostly in

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performed and insufficient amount
ranked second (10.88%), and spinach
of enhancers to bring up ID; (3)
koottu (mungbean dhal and spinach),
Group 3 vegetables such as tomato
and cabbage koottu (mungbean dhal
and pepper contained less inhibitors
and cabbage) ranked third and fourth
and more enhancers. Lack of apparent
with 10.6% and 10.1% iron
cooking enhancing effect was an
bioavailability, respectively. The
evidence of the lack of heat related
bioavailability of mungbean masial,
inhibitors, and high ID in both raw
which uses whole mungbean, recorded
and cooked forms explained the
bioavailability of 8.83%, compared to
existence of enhancers.
10.88% for the same recipe made with
mungbean dhal. A salad made with
The Applications
soaked mungbean dhal or sprouts
1. High-iron mungbean recipe design
achieved the same percent iron
for South India (Subramanian and
bioavailability as mungbean (whole
Yang, 1998; AVRDC, 1999): High–iron
mungbean) masial. Recipes made only
mungbean recipes were designed based
with rice and mungbean or mungbean
on the previous iron bioavailability
powder were found to have low iron
studies and traditional food prepar-
bioavailability. Recipes which included
ations in South India. The work was
no enhancing ingredient had low ID.
conducted through a joint effort by the
2. High-iron mungbean recipe design
researcher from India (Dr. M. A.
for North India (Bains, Yang and
Subramanian, Avinashilingam Deemed
Sundar, 2003): This work was
University, Coimbatore, India) and
conducted through a joint effort by the
researchers from AVRDC, Taiwan.
researcher from North India (Dr. Kiran
Fifteen recipes were designed
Bains, Department of Food and
using mungbean dhal (dehulled split)
Nutrition, Punjab Agricultural University,
and dehulled mungbean (dehulled split
Punjab, India) and researchers from
with hulls retained) as principal
AVRDC, Taiwan. The high iron recipes
ingredient in combination with
were prepared to suit the palate of
selected vegetables (Table 1). To
North Indians (Table 2). The selected
enhance the bioavailability of iron,
ingredients were inexpensive and easily
recipes should include one or more
assessable to rural families as well as
ingredients rich in ascorbic acid.
the urban poor.
Tomato mungbean dhal with rice was
3. Enhancing bioavailability of iron
determined to be the best in terms of
from mungbean and its effects on
ID (11.28%). Mungbean dhal masial
health of schoolchildren: The cooking
(mungbean dhal, tomato, onion)
enhancing effect could be extended to

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Yang and Tsou
Iron Bioavailability of Vegetables
115


Table 1. High-Iron Mungbean Recipes for
South India
Iron

Recipe name
Terms
Dialyzability

1. Mungbean Masial
Cooked legu

mes and vegetables mixed
8.83%
or mashed

2. Mungbean Dhal Masial


10.88%

3. Mungbean Dhal Koottu


Mixed vegetable curry with coconut
10.10%
with Cabbage

4. Dhal Koottu with
Moringa oleif
era, a high iron and
5.63%
Drumstick leaves
vitamin A tree vegeable

5. Mungbean Dhal Kootu with

6.95%
Amaranth

6. Dhal Koottu with Spinach


10.59%

7. Tomato Rice with Dhal


Dehulled split pulse
11.28%
8. Hot Pongal
5.76%

Harvest festival celebrated in Tamil

Nadu in January which lends its name to
two recipes in this book


9. Sweet Pongal

5.08%


10. Pesarattu
Mungbean dhal and rice pancake
9.33%
1 1. Tomato Adai


Rice and pulses soaked, ground and
9.71%
cooked as a pancake with various


ingredients for taste
12. Salad
8.78%


13. Pakoda
Small dough balls made from pulse and
5.06%


rice flour and onions, deep fried
14. Bonda
Large ball of legume flour dough deep
4%

fried


Data source: Subramanian and Yang, 1998



low ID vegetables and legume by
Dishes selected and modified based on
cooking together with high ID
availability and prices of ingredients at
vegetables such as tomato and Moringa
the local markets were identified and
(AVRDC, 2000; Yang et al., 2006).
used for the one year feeding trial
High iron mungbean recipes were
conducted among 225 school children
designed accordingly for south and
by Vijayalakshmi et al. (Avinashi-
north India (Subramanian and Yang,
lingam Institute for Home Science and
1998; Bains, Yang and Sundar, 2003).
Higher Education for Women ) in

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116 June 2006
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T
able 2. High-Iron Mungbean Recipes for

North India

Iron
Recipe name

Terms
Dialyzability

1. Dhuli Mung Dhal


Preparations made of split dehulled or
10.20%
whole pulse


2. Sabat Mung Dhal
Whole 8.15%

3. Parantha
Pancake

11.32%

4. Mung Dhal Khichri
A comb

ination of rice and legume
9.16%

5. Mung Spinach Saag
A

preparation of leafy vegetables
11.31%

6. Mung Amaranth Saag


11.24%

7. Mungbean Sprout Salad
Green gram,

vigna radiate var. radiata
10.66%

8. Sprouted Mungbean


Rice cooked with vegetables
8.82%
Pulao

9. Mung Sprout-Mint Raita
Fermented cu

rd with vegetables and
7.18%
species


10. Dahi Bhalla
Fermented and fried ball of mungbean in
9.55%
curd


11. Mung Spinach Pakoda
Fried snack prepared from vegetables
9.73%


coated with legume flour paste
12. Mung Namkeen
Fried and crispy snack prepared from
10.42%

legumes

13. Poha
Dish prepared from rice flakes and
10.70%


vegetables
Da ta source: Bains, Yang and Sundar, 2003

Southern India. The results indicated
traditional mungbean recipe (ID, 7%).
that mungbean supplementation
However, the one year feeding was
improved health parameters including
insufficient to raise the hemoglobin
clinical deficiency symptoms, body
level over the anemia level. The
weight index, hemoglobin level and
feeding trial demonstrated food-based
productivity (Vijayalakshmi et al.,
approach on cost-effective plant based
2003). Hemoglobin level increased
diet to improve iron deficiency, and
by10% for school boys and girls
suggested longer-term strategy to
receiving higher ID recipes (ID, 12%),
resolve sever anemia.
while by 5% increase of hemoglobin

level for the school children receiving

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