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Effect of Tea and Other Dietary Factors on IronAbsorptionItske M. Zijp a , Onno Korver a & Lilian B. M. Tijburg aa Unilever Research Vlaardingen, Vlaardingen, The Netherlands

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Critical Reviews in Food Science and Nutrition, 40(5):371–398 (2000)

Effect of Tea and Other Dietary Factors onIron Absorption

Itske M. Zijp,* Onno Korver, and Lilian B. M. Tijburg

Unilever Research Vlaardingen, Vlaardingen, The Netherlands

Referee: Prof. S. Seshadri, MS Univeristy of Baroda, Faculty of Home Science, Baroda 390 002 India

ABSTRACT: Iron deficiency is a major world health problem, that is, to a great extent, causedby poor iron absorption from the diet. Several dietary factors can influence this absorption.Absorption enhancing factors are ascorbic acid and meat, fish and poultry; inhibiting factors areplant components in vegetables, tea and coffee (e.g., polyphenols, phytates), and calcium. Afteridentifying these factors their individual impact on iron absorption is described. Specific attentionwas paid to the effects of tea on iron absorption.

We propose a calculation model that predicts iron absorption from a meal. Using this modelwe calculated the iron absorption from daily menus with varying amounts of enhancers andinhibitors.

From these calculations we conclude that the presence of sufficient amounts of iron absorp-tion enhancers (ascorbic acid, meat, fish, poultry, as present in most industrialized countries)overcomes inhibition of iron absorption from even large amounts of tea. In individuals with lowintakes of heme iron, low intakes of enhancing factors and/or high intakes of inhibitors, ironabsorption may be an issue. Depletion of iron stores enhances iron absorption, but this effect isnot adequate to compensate for the inhibition of iron absorption in such an inadequate dietarysituation.

For subjects at risk of iron deficiency, the following recommendations are made. Increaseheme-iron intake (this form of dietary iron present in meat fish and poultry is hardly influencedby other dietary factors with respect to its absorption); increase meal-time ascorbic acid intake;fortify foods with iron. Recommendations with respect to tea consumption (when in a criticalgroup) include: consume tea between meals instead of during the meal; simultaneously consumeascorbic acid and/or meat, fish and poultry.

KEY WORDS: bioavailability, daily menu, calculation model, deficiency.

* Address for correspondence: I. M. Zijp, Unilever Research Vlaardingen, P.O. Box 114, 3130 AC Vlaardingen,The Netherlands

I. INTRODUCTION

A. General

The human body contains about 50 mgiron per kg body weight (adults: 3 to 4 g ofiron). The major part (60%) is present ashemoglobin in erythrocytes in the blood andmyoglobin (10%) in muscle tissue. Hemo-

globin is a carrier of oxygen from the carrierfor muscle tissue. Iron is also a componentof several tissue enzymes such as cyto-chromes that are critical for energy produc-tion and enzymes involved in the immunesystem. Transferrin is the transport proteinthat takes care of iron transport through thebody. The storage of iron in the body occursas ferritin and hemosiderin, which occur

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widely in the tissues, with the highest con-centrations normally present in the liver,spleen, and bone marrow. Men in the devel-oped world have about 500 to 1000 mg ofiron stored as ferritin and hemosiderin.The iron stores in women seldom reach 500mg; 20 to 30% of women in Western indus-trialized countries usually have no iron storesat all. The average amount of iron stores inwomen in these countries can be estimatedto be around 150 mg.1

Exhaustion of iron stores by inadequateor impaired iron absorption or chronic bloodlosses can lead to iron deficiency and even-tually to iron deficiency anaemia. In bothconditions there is a lack of oxygen at cellu-lar level that, for example, can cause a re-duced physical working capacity. As iron isinvolved in brain development, iron defi-ciency also affects several brain functions(e.g., impairments in memory and learning).The effects of iron deficiency during infancyappear to be irreversible, while in older chil-dren the adverse effects are reversed. There-fore, some of the changes in brain functionmay be normalized by iron therapy, whereasothers, such as learning, do not seem to be

improved.1 The clinical parameters and theircut-off points used in the assessment of irondeficiency and iron deficiency anaemia arelisted in Table 1.

Iron deficiency is probably the most fre-quent nutritional disorder in the world. Around600 to 700 million of the world’s populationhave iron deficiency anaemia. Many morehave depleted iron stores and are at risk forthe development of anaemia. The highestprevalence is usually found in infants, chil-dren, teenagers, and pregnant women andwomen of childbearing age (Figure 1).

1. Losses and requirements

Iron is not actively excreted from thebody, a small amount is lost, mainly throughloss of blood and surface cells of the gut,urinary tract, and skin. In men this amountsto about 1 mg/d. In women additional lossesoccur through menstruation (0.5 mg/d), andthe cost of pregnancy (2 mg/d) and lactation(0.5 mg/d). The daily iron requirements fordifferent age categories listed in Table 2 andshown in Figure 2 are based on these losses.

TABLE 1Clinical Parameters to Assess a Subject’s Iron Status and the Cut-Off Points for IronDeficiency, Iron-Deficient Erythropoiesis and Iron Deficiency Anaemia20

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FIGURE 1. Percentage of population by age category in devel-oped and developing world with iron deficiency anaemia.37

TABLE 2Daily Iron Losses (mg) for Separate Age Categories33

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Assuming a mean iron absorption of10%, the recommended dietary allowance(RDA) for adults in the U.S.A. is set at 15mg iron per day.

II. IRON ABSORPTION

A. Iron in Food

There are two types of iron in food:heme iron and non-heme iron. Heme ironoccurs in meat, fish, and poultry. Non-hemeiron occurs in vegetable as well as in ani-mal products. The iron present in meatsconsists of 40% heme iron and 60% non-heme iron. Heme iron from hemoglobinand myoglobin in meat products usuallyconstitutes only 10% or less of the totaliron intake. Non-heme iron thus forms themain part of dietary iron intake.2 Heme ironenters the mucosal cells by a differentmechanism and is better absorbed than non-heme iron. Its absorption is also less influ-enced by the body iron status and is notaffected by other constituents in the diet(except for calcium).

Iron-rich foods are cocoa, liver, kidney,dried fish, shell-fish, sesame seed, soy flour,

and pulses. Iron-poor foods are milk, cheese,sugar, sweets, jams, and unfortified milledcereals.

B. Iron Balance

A subject’s iron balance differs betweenpersons and is dependent of several factors.The iron status of a person, and its dietaryhabits are important factors. Figure 3 givesan outline of all factors that might influenceone’s iron balance.

In healthy people iron overload rarelyoccurs. The amount of storage iron seldomexceeds 500 mg in women or 1500 mg inmen.1 When iron overload occurs, it is usu-ally caused by an inherited error in ironmetabolism (hereditary hemochromatosis) orwhen iron is administered as a parenteraliron preparation.3

Iron-deficient subjects absorb more ironfrom foods than subjects with sufficient ironstores. It is estimated that for an individualwithout iron stores, in total twice as muchiron is available as for an individual with500 mg iron storage.4 There is an inverselogarithmic relationship between iron storesand iron absorption rate.

FIGURE 2. Iron requirements for males and females vary during life. A Western diet, rich in meat and ironpromoters (— — —) is able to meet iron requirements of the majority of females at all ages except in infancy,at the peak of the pubertal growth spurt, and onset of menstruation and during pregnancies. In contrast, acereal-based diet, without meat or iron promoters and with excess inhibitors of iron absorption ( ), isnot able to meet the requirements of most childbearing women and some men. (Reproduced with permis-sion.20)

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The dietary form of iron (i.e., heme ornon-heme) plays a role in absorption andthus also in iron balance. Heme iron, whichis a porphyrin complex, is absorbed intactwithout releasing the iron in the lumen andtherefore the heme iron is not affected byother constituents of the diet. Because ofthis, the heme iron in the diet is usuallybetter absorbed than non-heme iron. Non-heme iron is present in foods as ferric andferrous salts. In the intestinal lumen the ironis released and rapidly chelated by otherconstituents in the food. The chelators canbe of two kinds: one class (“enhancers”)that forms soluble low-molecular-weightchelates that are absorbed easily, while theother class (“inhibitors”) forms insolublehigh molecular weight chelates that are un-available for absorption.

Contrary to the luminal factors that donot affect heme iron absorption, the mucosalregulation mechanism remains similar forheme and non heme iron. Interference at thisstage affects both heme and non-heme ironabsorption. Similarly, iron status of the indi-vidual also affects both heme and non-hemeiron absorption.

According to Monsen et al.,5 the absorp-tion of heme iron varies from 15 to 35% andnon-heme iron availability would lie between3 and 20%.5

Non-heme iron absorption-enhancingfactors are ascorbic acid, meat, fish, and poul-try and organic acids. Absorption-inhibitingfactors are phytates, tea, and coffee. Cal-cium is a dietary factor influencing both heme

and non-heme iron absorption. Inhibition bycalcium is not localized to the gastrointesti-nal lumen but to the mucosal cell itself.

In the section below, iron absorptioninfluencing dietary factors are discussed, theeffects of tea on iron absorption are dis-cussed separately in the following section.

C. Dietary Factors Influencing IronAbsorption

There are several dietary factors that in-fluence iron absorption. Both inhibiting andenhancing factors can be distinguished. In-hibitors are phenols, phytates, and calcium;enhancers are ascorbic acid and meat, fish,and poultry. All factors only affect the non-heme iron absorption. The only exception iscalcium, which affects both heme and non-heme iron absorption.

1. Polyphenols

Phenolic compounds bearing catecholgroups (e.g., catechin) or galloyl groups (e.g.,gallic acid) have marked iron-binding proper-ties. Tea, coffee, cocoa, red wine, many veg-etables (spinach), grains (red sorghum), herbsand spices (oregano, cinnamon) contain suchphenolic compounds and all have an in vitroinhibitory effect on iron absorption. Gillooly etal.6 found an inverse correlation (r = –0.901)between the content of condensed polyphenolsin vegetables and the iron absorption from them.

FIGURE 3. Relationships between Iron Absorption, Iron Requirements, Iron Balance, Iron Status, and IronStores

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For the greater part of these compoundsno research on in vivo inhibitory effects ofthese compounds on iron absorption has beenpublished. Coffee and tea have been exam-ined. Coffee is discussed here; tea is dis-cussed in a separate paragraph.

The inhibitory effect of drinking coffeeon iron absorption from a test meal wasinvestigated in four studies. Hallberg et al.7

found an inhibition of 24%, Morck et al.8 of39%, Derman et al.9 of 38%, and Brune etal.10 of 73%. The amounts of coffee con-sumed in these studies varied from 3 to 14 g(dry weight) in 150 to 250 mL coffee. Ingeneral, we assume a 40% inhibition of ab-sorption of the iron present in a meal by thesimultaneous consumption of ≥ 1 cup ofcoffee.

Several studies have shown that theinhibitory effect of polyphenols can bepartly counteracted by simultaneous con-sumption of ascorbic acid and meat, fish,and poultry.9,11 (See also paragraph onascorbic acid.)

The effect of tea on iron absorption isdiscussed in a separate paragraph.

2. Vitamin A

In a study by Layrisse et al.,12 it wasfound that the addition of vitamin A to abreakfast meal prevented the inhibiting ef-fect of simultaneously consumed coffee, tea,and phytates on iron absorption. Iron ab-sorption from nonenriched precooked maizebread was 3.0 and 6.0% in normal and iron-deficient subjects, whereas the iron absorp-tion from precooked maize bread with 1000IU of vitamin A/100 g flour (300 µg retinol/100 g flour) was 6.4 and 11.0% in normaland iron-deficient subjects, respectively. Vi-tamin A also prevented the inhibiting effectof polyphenols present in tea and coffee,which both reduced the iron absorption fromthe breakfast by more than 50% when givenalone.

3. Phytate

Phytates are a storage form of phos-phates and minerals in cereals, seeds, nuts,vegetables, and fruit. In the Western-typediet about 90% of phytates originate fromcereals. Bran, oats, and fiber-rich foodsare especially rich in phytates. Phytatesstrongly inhibit iron absorption in dose-dependent fashion and even rather smallamounts of phytate have a marked effect.In a study by Hallberg et al.,13 iron ab-sorption in human subjects was inhibitedby 18 to 82% when, 2 and 250 mg phytaterespectively, were added to wheat rolls.In studies by Brune et al.,14 Siegenberg etal.,15 and Rossander-Hulthén et al.16 (ap-pendix), a similar inhibitory effect wasfound.

The effect of phytate can also be coun-teracted by ascorbic acid, meat, fish andpoultry.

4. Calcium

Calcium as a salt as well as in dairyproducts markedly interferes with theabsorption of iron.17 The inhibition isequally strong for heme and non-hemeiron. Hallberg et al.18 describes thatthere is an inverse S-shaped relationbetween the amount of calcium in a mealand the inhibition of iron absorption;calcium amounts < 40 mg do not yetexhibit an inhibiting effect and amounts>300 mg do not further decrease ironabsorption.

Studies by Hallberg et al.7, 17, 19 andRossander et al.11 have shown that 15 to 20 gof cheese (containing 125 to 165 mg of cal-cium), one glass of milk (165 mg calcium),or 165 mg calcium as a salt inhibited ironabsorption by about 50%. The mean inhibi-tion by 125 to 165 mg calcium, calculatedfrom these studies was 46% (range: 26 to68%).

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In general, we assume that ≥ 100 mgcalcium inhibits both heme and non-hemeiron absorption by 50%.

5. Other Inorganic Elements

High doses of certain other inorganicelements (e.g., zinc, manganese, copper) alsointerfere with non-heme iron absorption; nor-mally, dietary sources alone are unlikely tobe high enough to have any adverse effect.20

6. Ascorbic Acid

Ascorbic acid is the most potent enhancerof iron absorption, both in natural and insynthetic form. Studies with different mealsshowed an exponential dose-dependent in-crease of non-heme iron absorption by in-creasing doses of ascorbic acid.21

Ascorbic acid is thought to enhance ironabsorption in the lumen of the gut. This keepsiron in a more soluble and absorbable formand prevents binding to inhibitory ligands.

When consumed simultaneously with tea,ascorbic acid can prevent the formation of aniron-tannin complex and thus counteract theinhibiting effect of tea on iron absorption.Siegenberg et al.15 concluded that about 50 mgascorbic acid is needed to counteract the effectof >100 mg tea flavonoids (100 mg tea fla-vonoids are equivalent to about 1/2 a cup of tea).

Ascorbic acid also counteracted the in-hibitory effect of phytates on iron absorp-tion.13 The neutralizing effect was related tothe amount of ascorbic acid given and theamount of phytates present. About 80 mgascorbic acid would be needed to fully coun-teract the inhibition of 25 mg phytate.

7. Meat, Fish, and Poultry

Meat, fish, and poultry promote non-heme iron absorption. The factor in meat

responsible for enhancing non-heme iron ab-sorption has not been identified. Presentevidence suggests that peptides rich in theamino acid cystein may play a role in theenhancement of non-heme iron absorption.22

Meat promotes iron nutrition in two ways: itstimulates the non-heme iron absorption andit provides the well-absorbed heme-iron. Ina study by Hallberg et al.23 the addition of75 g meat increased the absorption of non-heme iron about 2.5 times compared with abasal meal without meat. It is assumed that1 g of meat, fish, and poultry equals theenhancing effect of 1 mg ascorbic acid.5

8. Tea

The inhibiting effect of tea on non-hemeiron absorption is attributed to the tea fla-vonoids present in tea. Tea flavonoids arepolyphenols that contain two aromatic ringsas a functional group with two or more hy-droxyl groups. Molecules with an aromaticring with two hydroxyl groups (catecholgroup) or three hydroxyl groups (galloylgroup) positioned at adjacent carbon atomshave in vitro iron-binding capacities. Thereare several types of tea flavonoids: mono-mers (catechin), dimers (theaflavin), andpolymers (thearubigin). The thearubigins arepolymers of catechins and are called con-densed or non-hydrolysable tannins (Figure4). Black tea contains 10% flavonols, 25%catechins, 20% theaflavins and 45%thearubigins.

The mechanism of iron absorption in-hibition by tea is by formation of a com-plex of the tea flavonoids with iron. It ismainly the galloyl group in these phenoliccompounds that specifically binds iron.10

A cup of black tea, brewed with 2.5 g tealeaves contains about 200 mg tea fla-vonoids.24, 25 The molar ratio of tea fla-vonoids and iron is dependent of the pH;the ratio varies between 1:1 at pH = 2, 2:1at pH = 5.5, and 3:1 at pH = 8.0.24

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A few epidemiological studies havelooked at the relationship between tea con-sumption and the prevalence of anaemia.

Mehta et al.26 found that 4.2 and 6.2%,respectively, of men and women participat-ing in the American NHANES II study wereanaemic. It turned out that anaemic subjectsdrank less tea (3.1 cups/day) than normalsubjects (3.5 cups/day). However, intake ofthe iron absorption enhancing factor ascor-bic acid among anaemic subjects was sig-nificantly lower compared with normal sub-jects. Data on the intake of other enhancingor inhibiting factors were not given.

The study by Merhav et al.27 found op-posite results in their investigation of ironstatus of Israelian infants. They found anoverall frequency of anaemia of 48.4% anda tenfold higher prevalence of microcyticanaemia among tea-drinking infants com-pared with the control group not consumingtea. Ascorbic acid intakes were not deter-mined in this study.

Razagui et al.28 determined the iron sta-tus among 15 mentally handicapped men-struating women, a group with low food in-takes. They evaluated the relation betweentea consumption and iron status. It turnedout that there was a significantly higher teaintake during meals (563 ml/meal/d) by sub-jects with depleted iron stores, comparedwith women with sufficient amounts of iron(184 ml/meal/d). In this study, the meal-timeintake of vitamin C was also significantlylower in the anaemic subjects.

From these studies can be concluded thatin populations with inadequate diets or higher

iron needs (children) tea may reduce non-heme iron availability to a significant extent,especially when tea is ingested as part of adiet containing inadequate amounts of ascor-bic acid.

The inhibitory effect of tea on iron avail-ability is confirmed by human interventionstudies. Table 3 summarizes the studies inwhich the effect of black tea was investi-gated.

In human intervention studies in whichtea was used,8,10,29,30 iron absorption was in-hibited between 63 and 91%. The amount oftea flavonoids ranged from 40 to 420 mg percup of tea. The overview shows that therewas no major difference in inhibition be-tween different tea flavonoid concentrations.This suggests that the strength of the teadoes not have a major impact on the strengthof inhibition.

We conclude that iron absorption from atest meal is inhibited by about 60 to 70% inresponse to simultaneous consumption of onecup of weak, normal, or strong tea.

A cross-sectional study among a Japa-nese population showed that increased con-sumption of green tea was associated witha significant reduction in the mean serumferritin and hemoglobin concentrations (al-though all concentrations still fell withinnormal limits). The proportion of subjectswith anaemic hemoglobin concentrationswas not related to consumption of greentea.31

Unfortunately, we were not able to findhuman intervention studies investigating theeffect of green tea or black tea with milk.

FIGURE 4. Structure Formulas of Catechin, Theaflavin, and Thearubigin, a Condensed Tannin. R = galloylgroup.

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Studies on the time dependency of ironabsorption showed that tea consumption12 h prior to consumption of a test solutiondid not have an effect on the iron absorptionin rats.32 Nothing is known about tea con-sumption shortly before consumption of ameal. Disler et al.24 looked at the effect ofdifferent time intervals between iron and teaconsumption on the iron absorption inhibi-tion in rats. They found that the inhibitiondecreased from 62% (simultaneous consump-tion of tea and iron) to 30% (interval 0.5 h)to 21% (interval 1 h) to 10% and 15% (inter-val respectively 2 and 3 h). This suggeststhat tea only has a strong inhibitory effect oniron absorption when it is consumed with ameal and has a weaker inhibitory effect whenit is consumed between meals. From the studyby Disler et al.24 can be estimated that inhi-bition caused by between-meal tea consump-tion will be around 20%.

The latter two studies24,32 are rat studies.Reddy et al.30 have shown that rats generallyabsorb more iron than humans, because oftheir ability to synthesize ascorbic acid in

the gut, which promotes iron absorption. Al-though this makes the rat model not verysuitable to extrapolate results to humans itmay give an indication of the response inhumans, when human data are lacking.

The general conclusion on the inhibitoryeffect of tea on iron absorption in humanscan be formulated as follows: simultaneousconsumption of black tea and iron-contain-ing foods inhibits iron absorption by about60 to 70%, independently of the strength ofthe tea. Between-meal tea consumption in-hibits non-heme iron absorption by about20%.

III. MODELS PREDICTING DIETARYIRON ABSORPTION

In recent years, several models have beenintroduced to estimate iron availability (andthus absorption) from a diet, consideringenhancing and/or inhibiting factors presentin that diet. In the section below, four mod-els are discussed.

TABLE 3Overview of Studies in Which the Inhibiting Effect of Black Tea on Iron Absorption inHumans Was Investigated

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A. Model of Monsen et al.

Monsen et al.5 developed a model in whicha subject’s iron status, the intake of heme andnon-heme iron and the intake of ascorbic acidand meat, fish, and poultry were taken intoaccount. A subject’s iron status can vary be-tween 0 and 1000 mg iron stores with increas-ing heme and non-heme iron absorption atlower iron stores. Iron-status-related absorp-tion percentages as described by Monsen etal. are listed in Table 4.

The usefulness of this model is limitedbecause the effects of inhibitors such as teaand phytates are not considered. This might

lead to an overestimation of ironbioavailability.

B. FAO/WHO Model

The Food and Agriculture Organization(FAO) and the World Health Organization(WHO) suggested a model in which threecategories of usual diets are distinguished,each with a different iron bioavailabilitylevel.33

Low bioavailability diet (iron absorptionabout 5%): A simple monotonous diet contain-ing cereals, roots, and/or tubers and negligible

TABLE 4Percentage Absorption of Heme and Non-Heme Iron in Subjects with Different Levels ofIron Stores and Absorption-Enhancing Factors in the Diet.

Note: MFP = meat, fish, and poultry.5

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quantities of meat, fish, and poultry or ascorbicacid-rich foods. This diet contains large quanti-ties of foods that inhibit iron absorption such asmaize, beans, whole wheat flour, etc. and isdominant in many developing countries.

Intermediate bioavailability diet (ironabsorption about 10%): A diet consistingmainly of cereals, roots, and/or tubers andnegligible quantities of meat, fish, or poultryor ascorbic acid. A low bioavailability dietcan be raised to this level by increasing ab-sorption-enhancing foods. A highbioavailability diet can be reduced to thislevel by the regular consumption of ironabsorption-inhibiting foods such as tea orcoffee.

High bioavailability diet (iron absorp-tion about 15%): A diversified diet contain-ing generous quantities of meat, fish, andpoultry and/or ascorbic acid. This type ofdiet is typical for most industrialized coun-tries.

This model recognizes both inhibiting(phytate and tannins) and enhancing factors,but has its limitations as the descriptions ofthe diets remain strictly qualitative and thequantities of enhancers and inhibitors arenot defined.

C. Model of Murphy et al.

Murphy et al.34 combined the FAO/WHOand Monsen models to estimate iron absorp-

tion from diets in less-developed countries.It was assumed that 40% of all iron in meat,fish, and poultry is heme iron and that hem-iron bioavailability is 25%.

Rather than calculating iron bio-availability from each individual meal likeMonsen et al. did, Murphy et al. calculatediron bioavailability from food intake data ofan entire day. Furthermore, zero instead of500 mg iron stores were assumed. The pre-dicted impact of meat, fish, and poultry andascorbic acid were based on Monsen’s cut-off points (Table 4), non-heme bioavailabilityranging from 5 to 15% (Table 5). If anaemiais present, absorption would be increased by50%, to 7.5, 15, and 22.5%.33

In addition, a tea factor was used, rang-ing from 1 if no tea was consumed to 0.40for at least 600 mL tea/day.

The final algorithm was, available iron =heme iron × 0.25 + (non-heme × availabilityfactor × tea factor).

A limitation of this model is that effectsof phytates are not considered.

D. Model of Tseng et al.

Tseng et al.35 described a model to cal-culate iron availability, adjusting for dietaryascorbic acid, meat, fish, and poultry, tea,and phytate concentrations. They calculatediron availability for each individual mealthat leads to a more realistic picture of the

TABLE 5Bioavailability of Non-Heme Iron in Relation to Dietary Ascorbic Acidand Meat, Fish, and Poultry Concentrations

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amount of bioavailable iron than in the modelof Murphy et al.

In their calculations Tseng et al. usedabsorption estimates from Monsen et al.5

(Table 3), assuming that their study popula-tion had iron stores of 500 mg. In this waynon-heme iron absorption varied between3 and 8%, and heme iron absorption was setat 23%. It was assumed that 40% of the ironin meat, fish, and poultry was heme iron and60% was non-heme iron.

To adjust for the iron-absorption enhancingfactors (EF) present, the sum of grams meat,fish, and poultry and milligrams ascorbic acidwere calculated and inserted in an ascorbic acidand meat, fish, and poultry adjusted formula.*

When the sum of enhancing factors was <75,Then: Non-heme bioavailability (%) = 3 + 8.93ln [(EF+100)/100].

When this sum exceeded 75, non-hemebioavailability was set at 8%.

The availability percentage was adjustedfurther by correcting for tea and phytate con-sumption.

Non-heme iron bioavailability was in-hibited by 40% when the meal-time intakeof black tea exceeded 225 ml. To adjust forphytates, the tea-adjusted non-hemebioavailability was multiplied further by thephytate-adjusted availability percentage, cal-culated using the following formula**:log10(% non-heme bioavailability)= -0.2869× log10 (mg phytate in meal) + 0.1295

The final algorithm was, available iron =heme iron × 0.23 + (non-heme iron × en-hancing factors–adjusted availability factor× phytate adjusted availability factor × teafactor).

This formula calculates iron absorptionfor an individual with 500 mg iron stores.Note: In the case of depleted iron stores, thecalculated absorption percentage can bemultiplied by two to represent iron absorp-tion in an individual with zero iron stores.

This is relevant for many people in develop-ing countries.

A limitation of this approach might bethe adjustment for tea. As stated previously(Section B), a 60 to 70% inhibition at ≥ 150ml tea consumption seems realistic. How-ever, in this study iron availability was onlyadjusted when tea consumption exceeded 225ml and an inhibition of 40% was assumed.This procedure might lead to an overestima-tion of iron bioavailability.

E. A New Model

All models described in the section abovehave one or more limitations in their estima-tions of iron bioavailability. So far, the modelof Tseng et al. seems to be most realisticbecause it takes four dietary factors into ac-count (ascorbic acid, meat, fish and poultry,phytates, and tea), whereas the other modelsadjust for three or less factors or give onlyqualitative instead of quantitative descrip-tions.

However, the model of Tseng et al. stillseems to be inadequate for the prediction ofiron absorption from a test meal as coffeeand calcium also have a major impact oniron absorption. In this section a new modelis proposed.

In the appendix an overview is given ofstudies that measured iron absorption. Us-ing reference doses, all absorption percent-ages were recalculated to percentages rep-resentative for an individual with zero ironstores. When applying the model by Tsenget al. on these studies and multiplying thepercentages by two to adjust for zero ironstores, the calculated bioavailability figuresdo not always agree with measured absorp-tion percentages. Mean basic iron absorp-tion from a wheat roll without any enhanc-ing or inhibiting factors seems to be 22.5%

* Information on the origin of this formula was not given by Tseng et al.35

** This formula was derived by fitting data from Hallberg et al.13 into a logarithm regression model to estimateparameters

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in subjects with zero iron stores,10,13,14,17

whereas Tseng et al. calculate a basic ab-sorption of 6% from these wheat rolls (as-suming 0 mg iron stores).

An adjustment to the model of Tseng etal. could be the replacement of 3 by 22.5%in the formula of enhancing factors. In thisway a better estimation of basic absorptionis achieved. Calculated basic absorption canthen be adjusted further for tea, coffee,phytate, and calcium contents.

Another adjustment to the model ofTseng could be the implementation of ad-justments for coffee and calcium. In Sec-tion II.C iron absorption influencing di-etary factors were discussed. From thissection it appeared that coffee and calciumalso had distinct effects on iron availabil-ity. Coffee inhibited iron absorption byabout 40% and calcium had an inhibitoryeffect of 50%.

1. A New Model Could Be LookingAs Follows:

a. Assumptions Made

Iron in vegetable products: 100% is non-heme iron.

Iron in meat, fish and poultry: 40% isheme iron, 60% is non-heme iron.

b. Absorption of Heme Iron

35% absorption at zero iron stores: 17.5%if ≥ 100 mg calcium present in the meal.

c. Absorption of Non-Heme Iron

Basic absorption (%) from a test meal =22.5 + 8.93 * ln [(100 + EF)/100]

(maximum EF = 75, so maximum non-heme iron absorption = 27.5%).

This percentage is further adjusted for:

• Phytate effect:log (% absorption) =–0.2869 * log (mg phytate in a meal) +0.1295.

• Tea effect: 60% inhibition at ≥ 150 mLtea consumption when drunk with a meal.

• Coffee effect: 40% inhibition at ≥ 150 mLcoffee consumption when drunk with ameal.

• Calcium effect: 50% inhibition at ≥ 100mg calcium present in the meal.

The overview in the appendix also showsabsorption percentages calculated with thenew model. From this overview one of thestudies is selected and presented in Table 6to serve as an example.

In Table 6, measured and calculated ironabsorption from a study by Rossander et al.11

are compared. Iron absorption is calculatedin three different ways: according to Tseng’smodel, adjusted for 0 mg iron stores bymultiplying the outcome by 2, and accord-ing to the new model that assumes zero ironstores.

The new model gives reasonable esti-mates of iron absorption. In some cases theabsorption percentages as calculated byTseng’s method seem to be more accuratethan those calculated by the new model.However, in Tseng’s calculations coffee, tea,and calcium effects are not taken into ac-count so that in these cases the new methodstill is preferred.

When looking at studies investigatingthe sole effect of phytate or ascorbic acid(see appendix), it appears that the newmodel to a small extent underestimatesthe inhibiting effect of phytate and un-derestimates the enhancing effect of vita-min C. When investigating phytate ef-fects calculated absorption percentages arehigher than actual absorption and whenlooking at ascorbic acid effects the calcu-lated absorption percentages are lowerthan measured percentages. At this pointthe new model could still use some im-provement.

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However, when these two factors arecombined in a study, the underestimatingeffects cancel each other out so that the es-timated absorption reasonably well reflectsthe actual (measured) absorption. This is il-lustrated in the study by Siegenberg et al.15

(appendix).Overall, the new model gives better es-

timates of iron absorption than Tseng’smethod and absorption percentages calcu-lated with the new model could serve as anindication of real iron absorption from ameal.

IV. IRON ABSORPTION FROM ADAILY MENU

A. Four Daily Menus

In this section the impact of differentenhancing or inhibiting dietary factors oniron absorption from a daily menu are inves-tigated. Four countries with widely varyingdietary habits were chosen: England, theU.S.A., Russia, and India.

Using information on dietary habitsfrom travel guides, internet, market re-search reports and food compositiontables, a daily menu, typical for the coun-try, was composed. The term ‘typical dailymenu’ cannot be taken too literally be-cause within each country there are dif-ferences in dietary habits between differ-ent parts of that country. The menus thatwere chosen for this report consist offoods that were mentioned frequently astypical foods for a country in market re-search, travel guides, or the internet.Tables 7 to 10 give an overview of thefour daily menus.

From the menus iron content, ascorbicacid, meat, fish and poultry, tea, coffee,calcium, and phytate contents were calcu-lated using food composition tables, and,using this information, iron absorption wascalculated according to the new model asdescribed in Section III.E. All values arelisted in Tables 7 to 10. Apart from thesebioavailability calculations, the effect oniron absorption of drinking tea betweenmeals instead of during meals was also

TABLE 6Measured Iron Absorption (%) and Calculated Iron Absorption According tothe Model of Tseng,35 Assuming 0 and 500 mg Iron Stores and According to a NewModel Adjusting for Coffee and Calcium as Well

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assessed by calculating iron availabilitywith 20% inhibition of iron absorptioncaused by tea instead of a 60% inhibitionby tea. These values are listed in Tables 7to 10 as well.

B. Iron Absorption from DailyMenus

Calculated iron absorption from the fourdaily menus was 1.55 mg (12%) from the

TABLE 7English Daily Menu: Iron Content, Content of Enhancing and Inhibiting Factors andCalculated Iron Absorption from an English Daily Menu According to the New ModelProposed in Section III.F., Assuming 0 mg Iron Stores

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English, 1.75 mg (12.5%) from the Ameri-can, 0.66 mg (5.6%) from the Russian, and0.69 mg (4.9%) from the Indian menu.

The English and American menu pro-vided enough available iron for both menand women. Both diets contained a reason-able amount of meat and enhancing factorsand lower amounts of inhibiting factors. Thelow tea consumption in America may espe-cially contribute to a high iron availability.

The Russian and Indian menus were bothinadequate in providing enough available iron

for both men and women. Even though theRussian diet contained a significant amountof meat (165 g), the absorption was stillinadequate, probably because of high tea andphytate intakes. The Indian menu was lowerin meat products (100 g) and high in tea andphytate content, which also resulted in lowavailability. Although the ascorbic acid in-take (133 mg) was quite high, the major part(115 mg) originated from mango, which waseaten as a snack and thus did not enhanceiron absorption from lunch or dinner.

Table 8American Daily Menu: Iron Content, Content of Enhancing and Inhibiting Factors andCalculted Iron Absorption from an American Daily Menu According to the New ModelProposed in Section III.F., Assuming 0 mg Iron Stores

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C. The Effect of Between-Meal TeaConsumption

As stated in Section II.C., tea consump-tion has a smaller inhibitory effect on ironabsorption when consumed between meals(about 20%) than with meals (inhibition about60%). When calculating iron absorption as-suming that all tea is consumed after a mealinstead of with a meal, the absorption per-centages increase to 14% for the English

menu, 13.1% for the American menu, 7.1%for the Russian menu, and 7.5% for the In-dian menu. Despite changing to a betweenmeal tea consumption, the iron absorptionfrom the latter two diets still stays below theoptimum. A solution might be to increasemeal-time ascorbic acid intake, which in-creases iron absorption and counteracts theinhibitory effects of tea and phytates andthus elevates iron absorption to a more ad-equate level.

TABLE 9Russian Daily Menu: Iron Content, Content of Enhancing and Inhibiting Factors andCalculted Iron Absorption from a Russian Daily Menu According to the New ModelProposed in Section III.F., Assuming 0 mg Iron Stores

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V. GENERAL CONCLUSION

From the information given in this review,the following conclusions can be drawn. Asubject’s iron status is highly dependent on thebioavailability and thus absorption of iron fromthe diet. Iron absorption is markedly influenced

by meal-time intake of enhancing or inhibitingdietary factors. Especially ascorbic acid and meat,fish, and poultry as enhancers and tea, coffee,phytate and calcium as inhibitors have a greatimpact on iron absorption. Iron status of anindividual also influences iron bioavailabilityand shows an inverse relationship.

Table 10Indian Daily Menu: Iron Content, Content of Enhancing and Inhibiting Factors andCalculted Iron Absorption from an Indian Daily Menu According to the New ModelProposed in Section III.F., Assuming 0 mg Iron Stores

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Iron absorption is not a problem whensufficient amounts of heme iron and non-heme iron-enhancing factors (ascorbic acidand meat, fish, and poultry) are present in thediet. In individuals with lower intakes of hemeiron, lower intakes of enhancing factors and/or higher intakes of inhibitors such as phytate,tea, coffee, and calcium, iron absorption canbe a serious problem. Despite an increase iniron absorption when iron stores are depleted,this counteracting effect is inadequate to pro-vide a sufficient absorption. For women anadequate absorption is harder to achieve thanfor men, as their iron requirements are higherbut their iron-rich food intake is usually lower.Iron fortification of foods might be a solutionfor these people.

From the literature, four different mod-els to predict dietary iron absorption werereviewed. It appeared that the absorption es-timates from each model were limited be-cause in each model one or more major ab-sorption-influencing factors were not takeninto account. In response to these limita-tions, a new model to predict iron absorptionwas developed, taking all major factors intoaccount. After comparison with the resultsfrom existing iron bioavailability studies inhumans, it appeared that this new model canreasonably well predict dietary iron absorp-tion. This new model could be used as a toolto calculate the efficacy of iron fortificationof foods.

VI. RECOMMENDATIONS

As far as optimizing iron absorption fromthe diet is concerned, the following recom-mendations can be made.

A. General Recommendations

• Increase hem-iron intake. Heme-iron ab-sorption is only influenced by calciumand iron status and not by any other di-

etary factor. The absorption is relativelyhigh and meat, fish, and poultry enhancenon-heme iron absorption as well. Thisrecommendation is only suitable for indi-viduals with the means to buy more meat,fish, and poultry and where it is culturallyappropriate to consume meat.

• Increase meal-time ascorbic acid intake.Ascorbic acid enhances iron absorption tothe same extents as meat, fish, and poultryand can counteract the inhibitory effectsof phytates, tea, coffee, and calcium. In-creasing ascorbic acid intakes might beeasier to achieve in developing countriesthan increasing the intake of meat, fish,and poultry.

• Fortification of foods. In some countriesbreakfast cereals or other foods are forti-fied with iron. Fortification of foods couldbe a good method to increase iron intakein both developing and industrializedcountries. Furthermore, it is the onlymethod to increase iron intake for veg-etarian people, apart from maximizing thevitamin C consumption in their diet. Whenfortifying a food with iron, it should beattempted to reach an iron level that as-sures at least a 15% intake of the recom-mended daily allowance (RDA) per dailyserving of that fortified food.

B. Recommendations RegardingTea

• In countries with high heme iron intakeslike the U.K. and U.S.A., tea drinkingshould not be a problem, except for riskgroups (e.g., pregnant women, growingchildren). For these groups and for popu-lations in countries where the major ironintake is from non-heme iron the follow-ing recommendations regarding tea canbe made:

• Consumption of tea between meals in-stead of during the meal. Tea has a weakerinhibitory effect on iron absorption when

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it is consumed between meals. Alterna-tives for meal-time tea intake could bewater, fruit juice, or lemonade. When juiceis drunk containing ascorbic acid there isan additional beneficial effect on ironabsorption as ascorbic acid enhances ironabsorption.

• When tea is part of the meal, simulta-neously consume ascorbic acid and/ormeat, fish, and poultry. The inhibitory ef-fect of tea can partly be counteracted bythese enhancing factors.

ACKNOWLEDGMENT

The authors thank Loes Akerboom andMegan Cobcroft for their contribution to thisarticle.

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