Vitamin A and b-Carotene Can Improve Nonheme Iron Absorption fromMarı´a Nieves Garcı´a-Casal,* Miguel Layrisse,*‡3Liseti Solano,† Marı´a Adela Baro´n,† Franklin Arguello,† Daisy Llovera,
Trang 1Vitamin A and b-Carotene Can Improve Nonheme Iron Absorption from
Marı´a Nieves Garcı´a-Casal,* Miguel Layrisse,*‡3Liseti Solano,† Marı´a Adela Baro´n,†
Franklin Arguello,† Daisy Llovera,† Jose´ Ramı´rez,* Irene Leets* and Eleonora Tropper*
*Centro de Medicina Experimental, Laboratorio de Fisiopatologı´a, Instituto Venezolano de Investigaciones Cientı´ficas (IVIC), Caracas 1020A, Venezuela; †
Unidad de Investigaciones en Nutricio´n, Universidad de Carabobo, Valencia, Venezuela; and ‡
Universidad Central de Venezuela, Caracas, Venezuela
ABSTRACT After the rapid decrease in the prevalence of iron deficiency and iron-deficiency anemia in the
Venezuelan population when a national program for fortification of flours with iron and vitamins was instituted,
we studied micronutrient interactions in Venezuelan diets One hundred human adults were fed three cereal-based
diets, labelled with either 59
Fe or55
Fe in six studies Each diet contained different concentrations of vitamin A (from 0.37 to 2.78 mmol/100 g cereal) or b-carotene (from 0.58 to 2.06 mmol/100 g cereal) The presence of vitamin
A increased iron absorption up to twofold for rice, 0.8-fold for wheat and 1.4-fold for corn b-carotene increased
absorption more than threefold for rice and 1.8-fold for wheat and corn, suggesting that both compounds prevented
the inhibitory effect of phytates on iron absorption Increasing the doses of vitamin A or b-carotene did not further
significantly increase iron absorption We measured the iron remaining in solution performing in vitro studies in
which the pH of solutions was adjusted from 2 to 6 in the presence of vitamin A or b-carotene All of the iron
from ferrous fumarate was soluble after changing the pH of the solution containing 3.4 mmol of b-carotene to 6.0
Vitamin A was less effective However, 78{ 18% of iron was soluble in the presence of 3.3 mmol of vitamin A,
whereas with no vitamin addition, only 26 { 13% of iron was soluble (õ0.05) Vitamin A and b-carotene may
form a complex with iron, keeping it soluble in the intestinal lumen and preventing the inhibitory effect of phytates
and polyphenols on iron absorption J Nutr 128: 646 – 650, 1998
KEY WORDS: • iron • vitamin A • b-carotene • humans • phytates
Vitamin A is a vital nutrient for cellular differentiation, population (Taylor et al 1995), we continued studies of micro-vision, bone growth, reproduction and integrity of the immune nutrient interactions on iron ab sorption, especially since system (Olson 1984) It is also essential for erythropoiesis 1993, when the fortification of precooked corn and white Deficiency of this vitamin results in anemia in humans and wheat flours with iron and vitamins was started (Layrisse et animals that is reversed only by vitamin A supplementation al 1996)
(Bloem et al 1989, Hodges et al 1978, MejıBa 1986, MejıBa and The first experiments already were presented in two work-Arroyave 1982, MejıBa and Chew 1988, MejıBa et al 1979) shops (Casal and Layrisse 1996, Layrisse and
GarcıBa-b-carotene is the most abundant provitamin A in foods Casal 1997); and published (Layrisse et al 1997, Layrisse and Approximately 10 – 50% of the totalb-carotene consumed is GarcıBa 1997) The studies showed that addition of vitamin A absorbed in the gastrointestinal tract and within the intestinal (as retinol palmitate) and iron to corn or wheat flours used wall is partially converted into vitamin A The efficiency of to prepare a typical Venezuelan breakfast (basal breakfast)
b-carotene absorption decreases as intake increases and con- containing corn or wheat bread, cheese, margarine and coffee version to vitamin A is regulated by the vitamin A status of or tea, diminished the inhibitory effect of phytates and the individual.b-carotene accumulation is not toxic, so it is polyphenols on iron absorption
considered a safe source of vitamin A (Roche Laboratories We examined the effects of increasing doses of vitamin
1994, Wang 1994) A andb-carotene on nonheme iron absorption In addition, After reporting the results on iron availability from diets solubility changes of various iron compounds at pH 2 and 6 consumed by different socioeconomic strata of the Venezuelan with and without vitamin A andb-carotene are presented
MATERIALS AND METHODS
1 Supported in part by CONICIT, Caracas, Venezuela. One hundred and four adult subjects (27 men and 77 women from
2 The costs of publication of this article were defrayed in part by the payment
Valencia City, Venezuela) voluntarily participated in this study The
of page charges This article must therefore be hereby marked ‘‘advertisement’’
Committee for the Protection of Human Subjects of the Venezuelan
in accordance with 18 USC section 1734 solely to indicate this fact.
3 To whom correspondence should be addressed. Institute for Scientific Research approved the studies The subjects
0022-3166/98 $3.00 q 1997 American Society for Nutritional Sciences.
Manuscript received 4 June 1997 Initial revision completed 3 July 1997 Revision accepted 12 November 1997.
646
Trang 2TABLE 1
Composition of meals administered to human subjects participating in iron absorption studies
Meals 2
Test
n
1 17 Rice ( 59 Fe) 0.55mmol Vitamin A 1.51mmol Vitamin A 2.78mmol Vitamin A
( 55 Fe) ( 59 Fe) ( 55 Fe)
2 17 Corn ( 59 Fe) 0.37mmol Vitamin A 0.61mmol Vitamin A 0.73mmol Vitamin A
( 55 Fe) ( 59 Fe) ( 55 Fe)
3 20 Wheat ( 59 Fe) 1.10mmol Vitamin A 0.66mmol Vitamin A 1.51mmol Vitamin A
( 55 Fe) ( 59 Fe) ( 55 Fe)
4 11 Rice ( 59 Fe) 1.51mmol Vitamin A 0.58mmolb-carotene 0.95mmolb-carotene
( 55 Fe) / coffee ( 59 Fe) ( 55 Fe)
5 20 Corn ( 59 Fe) 0.61mmol Vitamin A 0.67mmolb-carotene 1.53mmolb-carotene
( 55 Fe) ( 59 Fe) / coffee ( 55 Fe)
6 19 Wheat ( 59 Fe) 0.66mmol Vitamin A 0.85mmolb-carotene 2.06mmolb-carotene
( 55 Fe) ( 59 Fe) / coffee ( 55 Fe)
1 Rice test: 100 g polished rice / 10 g margarine; corn test: 100 g precooked corn flour / 50 g cheese / 10 g margarine; wheat test: 100 g white wheat flour / 50 g cheese / 10 g margarine.
2 Parentheses enclose supplemented isotope.
were selected from a low socioeconomic stratum in a section of a estimated blood volume based on sex, weight and height (Nadler et
al 1962)
Venezuelan city They were in apparent good health, but some of
the women had moderate iron-deficiency anemia (hemoglobin õ120 The protocol for the administration of radioactive food in the
morning after an overnight fast and the afternoon of the same day g/L) Blood (30 ml) was taken from each subject in a tube with
ethylenediamine tetraacetic acid (EDTA) and kept refrigerated at was based on experiments previously published (Taylor et al 1995)
Four-hour intervals between meals are sufficient for iron absorption 47C until used to measure hemoglobin concentration (Crosby et al
1954), serum iron (International Committee for Standardization in studies
Chemical analysis. The total iron concentration of foods was Hematology 1978), unsaturated iron bin ding capacity (International
Committee for Standardization in Hematology 1978), serum ferritin determined by the digestion method (Bothwell et al 1979), phytates
by the method of Haug and Lantzsch (1983), tannate by the method concentration (Flowers et al 1986) and radioactivity measurements
(see next section) of Price and Butler (1977), vitamin A by the method of Strohecker
and Heming (1965) modified by Covenin (1989) and b-carotene by Three cereals were tested: corn, wheat and rice The corn test
contained bread from 100 g nonfortified precooked corn flour and 5 the method of Strohecker and Heming (1967)
Phytate concentrations in precooked corn flour, wheat flour and
mg iron as ferrous fumarate; the flour was given with 10 g margarine
and 50 g cheese The wheat test contained a bread prepared from rice were 257, 161 and 170 mg/100 g, respectively The mean tannin
concentration in coffee was 2500 mg/100 g In studies in which coffee
100 g of commercial white wheat flour enriched with 0.15 mg
thia-mine, 0.2 mg riboflavin, 2 mg niacin and 2 mg iron as ferrous fumarate was included, each subject consumed coffee prepared by the infusion
of 8 g of ground coffee beans
It also contained 10 g margarine and 50 g cheese The rice test
contained 100 g polished rice and was administered with 10 g marga- The mean iron concentration was 6 mg/100 g in the fortified
precooked corn flour, 3 mg/100 g in white wheat flour, and 4 mg/100 rine
Corn, wheat and rice tests were given alone or with different g in boiled rice The molar ratio of iron to phytate was 0.29 in
precooked corn flour, 0.23 in the wheat flour and 0.30 in boiled rice amounts of vitamin A or b-carotene The vitamin A used was
water-soluble retinol palmitate, and b-carotene was a 10% water-water-soluble
powder Both products kindly were supplied by Roche Laboratories
Absorption studies. Six studies were performed Each included
Ç20 randomly selected subjects The studies were designed to deter- Changes in added Vitamin A and b-carotene centration mine iron absorption from each test given alone in meal 1, and with
during preparation and cooking of meals 1
different amounts of vitamin A, b-carotene or coffee in meals 2 – 4
(Table 1).
After cooking procedures
Each subject was included in only one study Four meals were given
to each individual Radiolabeled iron was added to the water to prepare
Initially added Rice test Corn test Wheat test
the cereal Each meal contained either59Fe or55Fe (Table 1)
The first meal in each study was the corn, wheat or rice test given
mmol mmol per 100 g cereal
alone and administered after an overnight fast The second meal was
given in the afternoon of the same day Blood was drawn 15 d later
Vitamin A 1.1 (1000) 0.55 (496) 0.37 (338) 1.1 (1000) 2
to determine the hematological profile of the subjects and measure
2.2 (2000) 1.51 (1376) 0.61 (554) 0.66 (600)
the radioactivity of blood samples The subjects were fed again in
4.4 (4000) 2.78 (2526) 0.73 (661) 1.51 (1372)
the morning and in the afternoon of d 15 with meals 3 and 4, and
blood was drawn again on d 30 to measure the radioactivity in blood b-carotene 1.7 (1000) 0.58 (342) 0.67 (395) 0.85 (500)
and serum ferritin 3.4 (2000) 0.95 (558) 1.53 (902) 2.06 (1211)
Duplicate 10 ml blood samples and triplicate samples of the
radio-active foods were prepared for scintillation counting using the tech- 1Values are means, nÅ 3; numbers in parentheses are in IU
nique of Dern and Hart (1961a and 1961b) Iron absorption from 2 Vitamin A was not added to the dough It was dissolved in water
and administered, freshly prepared, as a beverage.
food was calculated from the radioactivity in the subject’s blood using
Trang 3Effect of increasing doses of vitamin A on iron absorption in humans from rice, corn and wheat tests 1
Iron absorption Subjects and Serum transferrin
gender 2 Hemoglobin saturation Serum ferritin Meal 1 3 Meal 2 Meal 3 Meal 4
6 M, 11 F 126 { 4 23 { 2 29 { 1 3.9 a { 1.1 8.4 b,c { 1.1 7.5 b { 1.2 11.7 c { 1.2
6 M, 11 F 135 { 5 27 { 2 28 { 1 5.8 a { 1.2 9.8 b { 1.2 13.9 c { 1.1 11.8 b,c { 1.1
3 M, 17 F 130 { 2 29 { 2 31 { 1 4.2 a { 1.2 7.4 b { 1.1 7.1 b { 1.1 7.5 b { 1.1
1 Values are means { SEM Means in a row with dissimilar letters are significantly different, Põ 0.05 Vitamin A was administered as a beverage while eating the bread in the wheat study, meal 2.
2 M, male; F, female.
3 No Vitamin A was added to any meal 1.
The mean tannin content in 8 g of coffee powder was 200 mg bion Laboratories, Clearfield, UT) were tested due to their stability
at alkaline pH
The molar ratio of iron to tannin content in the corn test was 1.0,
0.50 in the wheat test, and 0.66 in the rice test Iron solutions from each of the compounds mentioned, containing
5 mg of iron, were prepared in 0.1 mol/L HCl containing 0, 0.55, Because of the long distance between the laboratory and the place
were the experiments were performed, the meals were administered 1.1, 1.65, 2.2 and 3.3 mmol (0, 500, 1000, 1500, 2000 and 3000IU)
of vitamin A or 0, 0,85, 1.70, 2.55, 3,40 and 5.10 mmol (0, 500,
to the subjects 1 d after the meals were prepared Variations in added
vitamin A and b-carotene content due to cooking procedures are 1000, 1500, 2000 and 3000IU) of b-carotene A 2-ml aliquot was
taken to measure soluble iron at pH 2, and to the remaining solution,
shown in Table 2 In the case of the administration of 1.1 mmol
(1000IU) of vitamin A, the wheat bread was prepared separately, the pH was adjusted to 6 with careful addition of NaOH
After standing 10 min at room temperature, duplicate 1-ml aliquots and this amount of vitamin A was dissolved in 20 ml water and
drunk while eating the baked bread In a previous experiment, we from the top of the solution were taken, and iron was measured for all iron
compounds with different concentrations of vitamin A and b-carotene at demonstrated that ú80% of the vitamin A is lost during preparation
of the dough and baking procedures due to the effect of yeast and pH 2 and 6 by the digestion method (Bothwell et al 1979)
Statistical analysis. Paired t test was performed for iron
absorp-the prolonged heat (Layrisse et al 1997)
tion studies comparing all meals within each study It also was used
Solubility of iron compounds at pH 2 and pH 6. The effect of
to compare iron solubility at pH 2 and 6 in presence of vitamin A vitamin A and b-carotene on iron solubility at pH 2 and 6 was
or b-carotene
measured Four iron compounds were tested: ferrous sulfate, ferrous
fumarate, an iron-amino acid chelate (Ferrochel) and Ferric-sodium –
RESULTS
EDTA Ferrous sulfate was studied because it is a reference compound
Iron absorption studies. The effect of increasing doses of
for iron studies Fumarate is the salt used in Venezuela for enrichment
of corn and wheat flours Ferric-sodium – EDTA and Ferrochel (Al- vitamin A on nonheme iron absorption from meals containing
TABLE 4
Iron absorption from meals containing rice, corn or wheat given alone or administered with Vitamin A or b-carotene 1
Iron absorption Subjects and Serum transferrin
gender 2 Hemoglobin saturation Serum ferritin Meal 1 Meal 2 Meal 3 Meal 4
Vitamin A b-Carotene
mmol
3 M, 8 F 129 { 11 28 { 2 21 { 1 2.1 a { 1.1 4.6 b { 1.1 6.4 b,c { 1.1 8.8 c { 1.1
6 M, 14 F 130 { 11 30 { 2 24 { 1 3.0 a { 1.1 6.6 b { 1.2 8.5 b { 1.1 6.3 b { 1.2
3 M, 16 F 132 { 11 25 { 2 18 { 1 3.0 a { 1.1 5.5 b { 1.1 8.3 c { 1.1 8.4 c { 1.1
1 Values are means { SEM Means in a row with dissimilar letters are significantly different, Põ 0.05 Coffee infusion was administered with meal 3 for the rice meal and with meal 4 for the other two studies.
Trang 4TABLE 5
Effects of vitamin A content and pH on in vitro iron solubility
Ferrous fumarate Ferrous sulfate
pH Vitamin A 2 Fe Soluble iron Fe Soluble iron
2 — 3.87 { 0.1 b 100 { 2.6 6.18 { 0.4 b 100 { 6.5
6 — 0.99 { 0.2 a 25.6 { 5.2 2.24 { 0.2 a 36.2 { 3.2
6 0.55 (500) 1.32 { 0.3 a 34.1 { 7.8 3.33 { 0.1 a 53.9 { 1.6
6 1.10 (1000) 1.75 { 0.2 a 45.2 { 5.2 3.85 { 0.4 a 62.3 { 6.5
6 1.65 (1500) 1.90 { 0.2 a 49.1 { 5.2 3.88 { 0.2 a 62.8 { 3.2
6 2.20 (2000) 2.01 { 0.1 a 51.9 { 2.6 4.18 { 0.1 a 67.6 { 1.6
6 3.30 (3000) 3.0 { 0.5 b 77.5 { 12.9 5.47 { 0.3 b 88.5 { 4.9
1 Values are means { SEM, n Å 5 Means in a column with dissimilar letters are significantly different, P õ 0.05 Initial iron content: 5 mg.
2 Values in parentheses are in IU
rice, corn and wheat is shown in Table 3 Iron absorption creased as a function of vitamin concentration Iron solubility
increased in Ç20% with 1.1mmol (100IU) of vitamin A, and from the meal given alone was significantly lower than when
vitamin A was included There were no significant differences when 3.3mmol (3000IU) was added, solubility was Ç80%
Ferrous sulfate showed a similar pattern Iron solubility
de-in iron absorption from rice meals contade-inde-ing from 0.55 to
2.78 mmol (496 – 2526IU) vitamin A The same patterns of creased in 64% when pH was raised to 6 When vitamin A
was added iron solubility increased, and at 3.3 mmol (3000 iron absorption were observed from the tests containing pre
cooked corn flour and white wheat flour IU), iron solubility was near 90%
When b-carotene was added to ferrous fumarate solutions
In study 4, iron absorption from the rice meal containing
vitamin A (meal 2, Table 4), was more than double the absorp- at pH 2 and then raised to pH 6, virtually all of iron remained
in solution when 3.4mmol (2000IU) or 5.1mmol (3000 IU) tion from the meal given alone In the absorption test in which
the meal contained 0.58 and 0.95mmol (342 and 558IU)b- ofb-carotene was added (Table 6) For ferrous sulfate, 92%
of iron remained in solution at pH 6 when 5.1mmol (3000 carotene, iron absorption was more than two and three times
greater than the meal given alone The same pattern of iron IU) of b-carotene was added, whereas only 36% was soluble
at pH 6 without any provitamin addition
absorption was observed for corn and wheat tests The addition
of 8 g of coffee powder as a beverage to meal 3 for rice test Differences in percentage of soluble iron are not statistically
significant between ferrous fumarate and ferrous sulfate for the (0.58mmolb-carotene) and meal 4 for corn and wheat tests
(1.53 and 2.06mmolb-carotene, respectively) (Table 4), pro- same content of vitamin A or b-carotene, except for 0.55
mmol vitamin A or 0.85mmolb-carotene (P õ 0.05).
duced no difference in iron absorption compared with meals
with lower or higher content ofb-carotene and without coffee, It was not possible to observe an effect of vitamin A orb
-carotene on iron solubility for EDTA and Ferrochel because but the values were still significantly higher than those
ob-tained when the meal alone was consumed iron is 100% soluble at pH 6 without any vitamin addition
Iron solubility with pH changes. Changes in iron
solubil-ity when pH is raised from 2 to 6 in presence of vitamin A DISCUSSION
are shown in Table 5 For ferrous fumarate, pH increase
pro-duced a 75% decrease in iron solubility However, when vita- Vitamin A content is reduced to less than half during
cook-ing procedures, but this amount of vitamin A significantly min A was added and the pH raised to 6, iron solubility
in-TABLE 6
Effects of b-carotene content and pH on in vitro iron solubility
Ferrous fumarate Ferrous sulfate
pH b-Carotene 2 Fe Soluble iron Fe Soluble iron
2 — 3.78 { 0.1 d 100 { 2.6 6.25 { 0.1 e 100 { 1.6
6 — 0.99 { 0.1 a 26.2 { 2.6 2.24 { 0.3 a 35.8 { 4.8
6 0.85 (500) 1.00 { 0.2 a 26.5 { 5.3 2.57 { 0.1 a 41.1 { 1.6
6 1.70 (1000) 1.96 { 0.1 b 51.9 { 2.6 3.17 { 0.2 b 50.7 { 3.2
6 2.55 (1500) 3.18 { 0.1 c 84.1 { 2.6 3.57 { 0.2 c 57.1 { 3.2
6 3.40 (2000) 3.54 { 0.1 d 93.7 { 2.6 4.96 { 0.1 d 79.4 { 1.6
6 5.10 (3000) 3.81 { 0.1 d 100 { 2.6 5.74 { 0.1 e 91.8 { 1.6
1 Values are means { SEM, n Å 5 Values in a column with dissimilar letters are significantly different, P õ 0.05 Initial iron content: 5 mg.
2 Values in parentheses are in IU
Trang 5compared with these meals given alone It also shows that the ous liquid scintillation counting isotopes of55
Fe and 59
Fe as ferrous
perchlo-increase in doses from 0.37 to 2.78mmol (338 to 2526IU) did rate J Lab Clin Med 57: 322 – 330.
Dern, J R & Hart, W L (1961b) Studies with doubly labeled iron II Separation
not produce any further significant increase
of iron from blood samples and preparation of ferrous perchlorate for liquid
b-carotene has the same effect on iron absorption than
scintillation counting J Lab Clin Med 57: 460 – 467.
vitamin A In the case of rice meal, it was shown that 0.95 Flowers, C A., Kuizon, M., Beard, S L., Skikne, B S., Covell, A & Cook, J D.
(1986) A serum ferritin assay for prevalence studies of iron deficiency Am.
mmol (558 IU) ofb-carotene increases iron absorption more
J Hematol 23: 141 – 151.
than threefold compared with the meal given alone
Absorp-Garcı Ba-Casal, M & Layrisse M (1996) Fortificacio´n del hierro de los alimentos
tion from the other two cereals showed similar behavior It y su impacto sobre la deficiencia de hierro In: Anemia por deficiencia de
hierro en la regio´n Andina Definicio´n y estrategias de intervencio´n (Berger,
seems that b-carotene also prevents the inhibitory effect of
J., San Miguel, J., Arze, R., Fernandez, E., and Aguanyo, V., eds) pp 193 –
polyphenols on iron absorption When coffee was administered
200 Orstom, La Paz, Bolivia.
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Hodges, R., Sauberlich, H., Ganham, J., Wallace, D., Rucker, R., MejıBa, L &
withoutb-carotene or coffee Mohanram, M. (1978) Hematopoietic studies in vitamin A deficiency Am. Solubility tests demonstrated that vitamin A and b-caro- J Clin Nutr 31: 876 – 885.
International Committee for Standardization in Hematology (1978)
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fumarate This is may be due to a greater stability ofb-carotene International Committee for Standardization in Hematology (1978) The
mea-surement of total and saturated iron-binding capacity in serum Br J
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Results from solubility experiments as well as human
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improving iron absorption requires further studies to discover
Layrisse, M., Garcı Ba-Casal M., Solano, L., Baron, M., Arguello, F., Llovera, D.,
the mechanism for this peculiar reaction A previous publica- RamıBrez, J., Leets, I & Tropper, E (1997) The role of vitamin A on the
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nutrici-tography (HPLC) and solubility of iron with vitamin A at pH 6 onal In: Vitaminas, agentes nutritivos y terape´uticos (C Rozo and M Ma-suggest that vitamin A binds iron liberated during the digestive mome., eds.), pp 65 – 74 Ediciones Doyoma S.A Barcelona, Spain.
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