iron fortification an update

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P erspec tive in N u tr ition

The Am er ican Journal of C lin ic al N utrit ion 38 : OCTOBER 1983 , pp 648-6 59 . P rin ted in U SA 1983 Am erican Soc ie ty fo r C lin ica l N u tr ition

Iron fo rtifica tio n : an upda te 3Jam es D C ook, M D and M o lly E R eusser

ABSTRACT Iron fo rtifica tion is the op tim al app roach to reduc ing the h ig h preva lence ofiron defic iency in d ev e lo p ing coun tr ies . S elec tion of th e iron source en tails a com prom isebe tw een the u se of ine rt com pounds wh ich are poo rly absorbed and ch em ica lly reac tive fo rm sw ith h igh b ioava ilab ility . A ltho ugh the veh ic le and fo rtif ica tion com pound m u st be cho sen intandem because m ost iron com pounds cau se d isco lo ra tion o r ranc id ity , the em phas is in th isrev iew is on the food v eh ic le . T ech no logy fo r fo rtify ing w heat flou r and bread is w ell estab lish edand the use of th ese v eh ic les has pro bab ly had a s ign ifican t im pac t on iron sta tus in W este rncoun tries . R ecen t s tud ies in Ind ia ind ica te th at th e fo rtifica tion of comm on salt is techn ica llyfeasib le and fie ld tr ia ls have show n a good hem ato log ica l respo nse . S im ilar success has beenach ieved by fo rtify ing ref in ed sugar w ith N aF eEDTA in Guatem ala . R ice has adv an tages as aveh ic le in those areas w here it is the s tap le foo d bu t th e techno log y requ ires fu rthe r deve lopm en t.F ish -based cond im en ts h ave been success fu lly fo rtified w ith N aF eED TA and show prom ise as aveh ic le in E ast A s ian coun tries. T he fo rtifica tion of in fan t foods po ses no techn ica l p rob lem s andshou ld be encou raged . A dd itio na l w ork is needed to id en tify o th er fo rtifica tion op tions and todeve lop ta rg eted fo rtif ica tion program s th a t w ill d irec t iro n to tho se segm ents o f a popu la tion ingrea test need . Am J C lin N u tr 1983 :38 :648-659 .K EY W ORDS Iron fo rtifica tion , iron defic iency

Introduction

N u tritio na l iron d efic iency is a m a jo rhea lth p ro b lem in deve lo p in g co un trie s. T h eo n ly p rov en w ay it c an b e a llev ia ted is toin cre a se iro n in take , e ithe r by p rov id ing m e-d ic ina l iro n (sup p lem en tation ) o r b y add ingiro n to th e d ie t (fo rtif ic a tion ) (1 ). Iron su p -p lem en tation ha s the ad van tage o f p rod uc -ing rap id ch an ge s in iro n s ta tu s and o f d i-re c ting iro n to tho se segm en ts o f a po pu la-tio n in g reate s t n eed . H ow eve r, its e ffec tiv e-n e ss is lim ited b ecau se o fthe ga s tro in te st ina ls ide e ffe cts o f o ra l iron and the d ifficu lty insus ta in in g m o tiv ation o f the pa rtic ip an ts .M oreove r, iron sup p lem en tat ion requ ires aneffe c tive sys tem of h ea lth d elive ry an d isco s tly to m ain ta in .

F o rtif ic a t ion is gen era lly con s ide red th ebe s t lo ng -term appro ach fo r com batt ing iro nd efic iency . It re a ch es a ll segm en ts o f th epo pu la t ion and doe s n o t requ ire the co op -64 8

e ra t ion o f the ind iv idu al. T he in itia l cos t ism od es t an d the m a in ten an ce ex pense is fanle ss than th at o fsu pp lem en ta tio n . H ow eve r,th ere are m any tech n ic a l d ifficu l tie s in fo r-ti fy in g th e d ie t w ith iron , th e m o st im po rtan tb ein g th e id en tific a tion o f a fo rm o f irontha t is adeq ua te ly ab so rbed an d y et d oe s no ta lte r the app ea rance o r tas te o f th e foo dv eh ic le . B ecau se no s in g le fo rtif ic a tio n s tra t-egy is su i tab le fo r w orld -w ide use , reduc in gth e g lo ba l p reva lence o fa nu tritio na l anem iaw ill req u ire th e deve lopm en t o f sev era l op -

I From the In te rna tiona l C en te r fo r C on tro l o f N u -tritio na l A n em ia , D iv is io n o f H em ato lo gy /D ep artm en to f M edic ine , U niversity o f K an sas M edica l C en te r,K an sas C ity , KS .

2 Supported by USA ID C oopera tive A greem en tDAN -0227-A -00-2 104-0 0 .

3 Address rep rin t reques ts to : D r Jam es C ook , U ni-vers ity o f K ansas M edica l C en te r, 39 th and R ainbowBou levard , K ansas C ity , K S 66103 .

R ece ived A pril 1 1 , 1 983 .A ccep ted fo r pu b lica tion A pril 12 , 19 83 .


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stances; discoloration is a particular problemwhen fortifying white foods such as refinedsugar, rice, and salt. I n addition, reactiveiron compounds catalyze oxidative reactionsresulting in undesirable odors and flavors.W hen these organoleptic problems developslowly, the shelf-life of packaged food vehi-des such as flour and processed cereals isreduced.

Common iron sources and their relativecosts are presented in T able 1 . T he solublecompounds are both the best absorbed andthe most chemically reactive. Because of thehigh bioavailability of ferrous sulfate, it isused extensively to fortify foods such asbread and bakery products which are storedfor only short periods of time. Ferrous fu-marate is used to fortify corn-soy-milk, aprotein supplement and weaning food sup-plied by the U SA in international food as-sistance programs. T he absorption of ferrousfumarate is comparable to ferrous sulfatewhen given at therapeutic levels withoutfood (5 , 6), but is apparently less when addedto food (H allberg L , personal communica-tion). Ferrous lactate and ferrous gluconateare well absorbed but their cost generallylimits their use to milk and soy-based for-

tions from which a given country or regioncan select. T he purpose of this report is toreview current information on iron fortifi-cation with particular emphasis on thechoice of the food vehicle.I r on c o mp o un d s

T he success of iron fortification dependsas much on the fortification compound ason the food vehicle. Fortification with ironis technically more difficult than with othernutrients because bioavailable forms of ironare chemically reactive and often produceundesirable effects when added into the diet.Since the population will seldom accept thefortified vehicle if the added iron can bedetected, inert iron compounds are com-monly used, but these are poorly absorbedand have little effect on iron status. A criticalstep in the design of an iron fortificationprogram is the selection of an iron com-pound that is both unobtrusive and wellabsorbed.

I deally, bioavailability of fortification ironshould be determined by labeling the prod-uct isotopically and measuring its absorptionfrom the diet in human subjects. H owever,because of the complexity of isotopic meas-urements in humans, bioavailability of ironcompounds is often based on animal studiessuch as the H b repletion method (2, 3). I nthis approach, H b response to graded irondoses is measured in iron-deficient rats andcompared to that observed with ferrous sul-fate, the accepted standard in iron availabil-ity studies. Since even animal assays are toocumbersome for routine monitoring of bioa-vailability of different commercial ironsources, simple in vitro techniques such asparticle size, dissolution rate in hydrochloricacid, or reactive surface area are commonlyemployed; the latter appear to be better pre-dictons of iron absorption than particle size(4). A major concern with both animal andphysical measurements of bioavailability isthat their precise relationship to absorptionin humans has not been adequately defined.

Bioavailable sources of iron pose seriousproblems to the food manufacturer. Solubleferrous salts often produce color changes byforming complexes with sulfur compounds,tannins, polyphenols, and other food sub-

Relativecost*

S7

117

617

1.51. 51. 5

11* I ncorporates purchase price, percentage iron, and

bioavailability. V alues expressed relative to ferrous sul-fate.

I RO N FO RT I FI CA T I O N : U PD A T E 649

T A B L E 1I ron compounds used for fortification

I . S ol ub leI . F errou s su lf ate2. F errous f um arate3. F errous lactate4. F errous gl uconate5. Ferric ammonium citrate

I I . P hospha te1 . Fer ri c ort hophosphat e2. Sodium f erri c pyrophosphate3 . F er ri c p yr op ho sp hate

I I . E lem en tal1 . R educed iron (hydrogen, CO )2 . Electrolyt ic3 . C a rbonyl

I V . C omplex1.2.


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6 5 0 COOK A N D R EU S S ERm ulas . Fe rric am m onium c itrate is usedcom m only in in f an t f o rm u las and has b eenused in th e U K f or f orti f icatio n o f w h eatf lou r. A bso rp tion o f th is iro n sou rce w asrepo rted to be poor in h um an su b jec ts w h enbak ed in to bread (7 ) o r added to w h eatch apatt i (8 ), bu t com parab le to that o f f e r-n ou s su lf ate in anem ic rats (9 ); th ere is ap -p aren tly con s ide rab le v ariation in b ioav ail-ab ility b etw een d if f e ren t com m erc ial pro d -ucts .

Phosphate com pounds are at the oppo s iteen d o f the spectrum in reg ard to b io av aila-b ility an d o rgano lep tic pro b lem s . Fe rric or-tho pho sphate and so d ium py ropho sphatew ere u sed ex tens iv ely f o r f lo ur an d cerealf o rtif icatio n in th e U S A because o f th eir lowco s t an d low v eh ic le reac tiv i ty , b u t the ir us edeclined w h en iso to p ic stud ies in hum ansu b je c ts sh ow ed ab sorp tion to be f ar le ssthan that o f f e rro us su lf ate ( 1 0 , 1 1 ). Ferricorth opho sp hate is s till in use b u t its re lativ eb io log ical v alu e (abso rp tion re lativ e to f e r-ro us su lf ate ) is h igh ly v ariab le , ran g in g f rom5 to ov e r 60 d ep end in g on th e com m ercialb atch (1 2 -14 ). T he relativ e cos t o f th e se ironf o rm s is h ig h b ecause o f po or av ailab ility .

Elemental iron pow ders, w hich o ccup y anin te rm ed iate po si tion be tw een the so lub lean d phosphate g ro up s in regard to ab sorp -t ion and reac tiv ity , hav e b een used ex ten -s iv e ly f o r f o rtif ication o f f lo ur an d bread inthe U S A and E uro pe . S u rf ace area, b io a-v ailab ility , and co st are low est f o r hy d ro genand CO -red uced iro n , in te rm ed iate f o r dcc-tro ly tic iro n , and h ig hest f o r carbony l iron ,bu t th e d if f e rences are n o t pro noun ced (3 ).S eg reg ation o f the se h igh dens ity iron p rod -u c ts m ay be a p ro b lem w ith som e v eh ic le s ,an d h ig h ly puri f ied and f in ely p ow dered iro nis p y rop ho ric (1 5). T he phy s ical p rop ert iesan d b ioav ailab il ity o f f o od grade e lem en taliron pow ders hav e b een rev iew ed in de taile lsew here(l6 , 17 ).

A complex in w h ich iron is tig h tly bo undm igh t m in im iz e ad v e rse reac tion s w ith af o od v eh ic le bu t , u n f o rtun ate ly , m os t ironch elatin g sub s tan ce s com pe te w ith th e in tc s -tinal m ucosa f o r iron . O n e ex cep tion isE DT A w hich im pairs ab so rp tion in h ig hco ncen tration s (1 8 ) bu t m ay actu ally en -h ance ab sorp tion w h en added in eq u im o larco ncen tration s as in the case o f so d ium ironED T A (N aFeED T A ) ( 1 9, 20 ). N aFeED T A

m in im iz e s the pro b lem o f iro n p rec ip i tationth at o ccurs w hen f ish sauce is f o rtif ied w ithiron (2 1 ) and w hen f ort if ied sug ar is add edto tea (2 2 ). A no the r org an ic com p lex , d riedH b , has ex cep tion ally h ig h b ioav ailab il itybu t im parts an in ten se co lor to f oo d andreq u ires a co n tin u in g supp ly o f an im alb lood .

S om e o f the tech n ical prob lem s that occu rw ith f oo d iro n f o rtif ication m ig h t be c ircum -v en ted b y u s ing a re lativ e ly in ert f o rm o firon in com b in ation w ith a subs tan ce th atenhan ce s ab so rp tion su ch as ascorb ic acid .T he com bin ation o f a s tab iliz in g agen t tored uce the react iv ity o f iro n durin g s torageand an acid if y ing agen t to enhan ce av aila-b i lity at the tim e o f in ge s tion has b een u sedto adv an tag e in th e f orti f icatio n o f com m onsalt . Fort if icatio n w ith ascorb ic acid alon em ay im p rov e iron nu tritu re bu t th e cos t o fadd ing it to th e f o od supp ly o f an en tirenatio n w ou ld b e p roh ib it iv e .Food veh ic l e s

A lthou gh th e iron f o rtif ican t an d f o odv eh ic le m ust be ch osen in tan dem , th e latte ris m ore im portan t. In se lec tin g th e v eh ic le ,con s ide ration m ust be g iv en to bo th th epatte rn o f its co nsum ptio n and the techn icalf eas ib ility o f its f o rti f icatio n (T ab le 2 ). T h ev eh ic le m ust reach a h ig h pro po rtion o f th ev u lne rab le p opu latio n and b e co nsum edev en ly th rou ghou t th e reg ion o r coun try .A ny eco nom ic b ias in v eh ic le consum p tio nshou ld f av o r low incom e g roups in w h ichT A B L E 2C ons id eration s f o r se lec tion o f f oo d v eh icleCo n s ump t i o n

H ig h p roportion o f pop u lationM in im al reg ional v ariationU nre lated to soc ioeconom ic s tatu sM in im al v ariation b etw een ind iv id ualsL ow po ten tial f o r ex cessiv e in tak eC on tain ed in all m ealsL ink ed to calo ric in tak e

Techn ica lC en trally p ro ce sse dFew produc tion f ac ilitie sG ood m ask ing qualitie sL ow cos tM in im al s eg re gatio nL im ited s to rage tim eH i gh b io av ai lab il it yN o nu trien t in te rac tio ns


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lRO rOR T I FI CA T I ON : U PD A T F ( 5 1nutritional anemia is more prevalent. I t isimportant that the supply of iron be rela-lively constant to both the household andthe individual and that there be little chanceof some people consuming large amounts ofthe fortified vehicle as might occur with softdrinks or snack foods. I deally, the vehicleshould be a component of all meals becausepercentage absorption varies inversely withthe iron content of the meal.

T here are also several technical consider-ations in selecting a vehicle. I t must be cen-trally processed to permit an entry point foriron, a factor that limits the use of homegrown foods. T he fewer the number of pro-duction facilities, the easier the task of mon-itoring the fortification process. Food vehi-des that are dark in color or have a strongtaste or odor permit the use of more reactiveiron compounds. T he vehicle should not beexpensive nor should fortification greatly in-crease the purchase price. Segregation ofiron during mixing or storage can occur withsome vehicles, and organoleptic problemsare lessened with vehicles that do not requireprolonged storage, particularly if the climateis hot and humid. Substances that inhibitiron absorption, such as coffee (23), wouldnot be suitable vehicles. I deally, the vehicleshould not contain other nutrients such asiodide that are affected by the added iron.Obviously, many trade-offs are involved inselecting vehicles for iron fortification.Wheat

W heat flour and bakery products deservecareful consideration because of the techni-cal success of their fortification in Europeand N orth A merica. Fortification iron inwheat flour and bread account for about20% of the iron intake in the U SA andnearly twice this amount in Sweden. A l-though the efficacy of fortifying bread withiron has not been firmly established, the highlevel of iron added to the Swedish diet isconsidered an important factor in themarked reduction in the prevalence of ane-mia during the past 10 to 1 5 yr (24). T hequestionable efficacy of flour fortification inthe U K (25) may relate to the use of poorlyabsorbed forms of iron. I n developing coun-tries where wheat is a staple food, it is anattractive vehicle because it reaches all seg-ments of the population, provides a rela-

tively even meal distribution of the addediron, and furnishes a reasonably constantiron supply to each individual. For example,based on food consumption data in Cana-dian women, it was predicted that with in-creased bread and wheat fortification, thedifference between the 10th and 90th per-centile in individual iron intake would beless than 2-fold (26). A nother advantage ofusing wheat and bread as vehicles is that thebioavailability of iron added to high extrac-tion wheat flour is several times greater thanthat added to other staple foods such asmaize and rice (27). T his is less importantw ith large meals but could be an advantagewith snacks in which most of the caloriesare derived from wheat flour.

T he problem of reduced shelf-l ife is oflittle concern when fortifying bread and bak-c ry products because they are consumedpromptly. I n fact, pilot studies have mdi-cated that there would be little difficulty intripling the current level of bread fortifica-tion in the U SA using highly available fer-rous sulfate (28). W hen flour is fortified withsoluble iron sources changes in color, odor,and taste occur, a problem that has beenlargely eliminated by using elemental iron.T his form of iron may segregate when flouris handled in bulk with pneumatic convey-ing systems and may be extracted by themagnets used to remove contaminants dun-ing milling. W heat flour and wheat productsappear to be the best vehicles for iron inregions such as Egypt and the Caribbeanwhere wheat is the staple food. A draw backin many T hird W orld countries is that mostofthe wheat flour is imported and consump-tion usually favors the higher income seg-ments of the population. U nfortunately,wheat is not a staple food in many areas ofthe world where nutritional anemia is highlyp r e v a l e n t .Salt

T he use of salt as a vehicle for iodide hasbeen successful in eradicating endemic goi-ter and it may be the optimal vehicle foriron fortification in many countries. Refinedsalt provides a relatively constant intake foreach individual, has little potential for cx-cessive intake, is consumed by most of thepopulation, and is not limited to the higherincome segments. I t is the only iron vehicle


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652 CO O K A N D R EU SSERthat is feasible in I ndia because it is one ofthe few dietary items that is centrally proc-essed. H owever, in certain coastal regionssalt is obtained locally by solar evaporationof sea water and bypasses industrial process-ing. I n the Philippines, fortification of re-fined salt is considered impractical becauseintake favors the higher socioeconomicstrata.

T he fortification of salt is beset by formi-dable technical problems. T he overridingdifficulty is that bioavailable forms of ironproduce unacceptable changes in color, es-pecially w ith less refined cooking salts be-cause ofthcir high moisture content. I n hot,humid climates the iron may actually gray-itate to the bottom of the storage container,leaving the upper layer of the vehicle iron-free and the lower layer with potentiallyharmful quantities (29). Salt fortification hasbeen studied in I ndia for several years. I ronabsorption measurements have shown thatfortification with sodium iron pyrophos-phate, fernic orthophosphate, or ferric pyro-phosphate is unacceptable because of lowbioavailability (30). Efforts have thereforefocused on the use of one of these inert ironcompounds in combination with substancesthat promote absorption. South A fricanworkers have shown that the combinationof fernic orthophosphate, starch, and ascor-bic acid is technically feasible and ensuresadequate assimilation, although the cost ofascorbic acid may be prohibitive (3 1 , 32).T he combination of ferrous sulfate, sodiumhexametasulfate (stabilizer) , and sodiumacid sulfate (enhancer) is also technicallyfeasible but again the cost is relatively high(33, 34). Ferrous sulfate and orthophos-phoric acid are adequately absorbed, butsome deterioration of bioavailability occursduring storage due to the formation of in-soluble iron phosphates (35) . NaFeEDTAprovides adequate amounts of iron but itdiscolors refined salt and is relatively expen-sive.T he combination offerric orthophosphateand sodium acid sulfate has recently beenreported to produce acceptable long-termbioavailability of the added iron with onlyslight discoloration, even under adverse stor-age conditions (36). T he cost ofthis strategycan be reduced further by using ferrous sul-fate, orthophosphoric acid (color stabilizer),

and sodium acid sulfate (enhancer). I n re-cent field trials in I ndia, common salt wasfortified in this manner to a level that pro-vided an additional iron intake in adults of10 to 15 mg/day (37). T he salt was fortified

by crushing to a coarse pow der and batchmixing it w ith the three chemicals to achievean iron content of 1 mg/g. D iscolorationwas minimal except when poor quality saltw ith a moisture content above 10% wasused. Ordinary gunny sacks used for pack-aging and transportation proved unworkablebecause of the corrosive nature of the addedchemicals but this problem was eliminatedby using unlaminated high-density polyeth-ylene. T he product was tested for 1 2 to 18months in one urban and three rural areas,and was well accepted except in some areaswhere the population was not accustomedto using crushed salt. W here the prevalenceof anemia was high, a gratifying improve-ment in H b levels was observed. T he cost offortification, which increased the cost of saltby about 20% , was estimated at about U S$0.07/person/yr. T hese findings indicatethat common salt merits strong considera-tion as a vehicle for iron.Suga r

Sugar, which has been used successfullyfor vitamin A fortification, has been pro-posed as a vehicle for iron (38-4 1) becauseits intake is relatively constant for each in-dividual and it reaches a high proportion ofthe population. Pilot fortification studieshave used highly refined sugar because in-dustrial grade sugar has a greater potentialfor idiosyncratic consumption. I ron addedto sugar would be well absorbed, especiallyifconsumed in citrus drinks, although a highproportion of sugar intake in adults is withtea and coffee which impair iron absorption.Sugar is an attractive vehicle in regions suchas the Caribbean and Central A merica whereit is produced, but in many developing coun-tries refined sugar consumption favors themiddle and upper economic segments of thepopulation (42). A s with salt, the main tech-nical drawback to using sugar is in selectingan available form of iron that does notdarken the product. A dditional problemsinclude segregation, which may reduce theshelf-life of less refined products with highmoisture content, and the immediate dis-


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I R ON FOR T I FI CA T I ON : U PD A T E 653

coloration that occurs when iron fortifiedsugar is added to tea.

Some of these obstacles have been sur-mounted by using N aFeED T A as the forti-fying agent (20). T his iron compound im-parts a very slight yellowish tinge to refinedsugar and greatly retards discoloration whenthe fortified product is added to tea. Segre-gation has not been a problem with whitesugar because N aFeED T A sticks to the crys-tal when moisture content is above 1 % . Akey advantage of N aFeED T A is its highbioavailability. A bsorption from this com-plex is 1 .5 to 2 times higher than from nativedietary iron in a cereal meal and may ac-tually facilitate absorption of nonheme ironin meals oflow bioavailability. On the otherhand, N aFeED T A reduces the facilitatingeffect of ascorbic acid on iron absorptionand does not fully escape the action of stronginhibitors such as tea (19).

Preliminary analysis of an extensive fieldstudy with N aFeED T A -fortified sugar inGuatemala has shown significant improve-ment in iron status (4 1). Fortification wasfound to be technically feasible and accept-ance by the population was good. N o ad-verse effects of this chelate on other divalentcation nutrients such zinc, copper, and man-ganese have been seen and there are nounfavorable interactions when sugar is for-rifled simultaneously with encapsulated vi-tamin A and iron. H owever, N aFeED T A issomewhat more costly than other fortifica-tion strategies. T he addition of sufficientiron to sugar to increase iron intake in anadult woman by about 5 mg iron daily (13mg iron/lOO g sugar) would cost approxi-mately U S $0. 1 0/person/yr although thecost of the vehicle itself would be increasedby only about 1 to 2% . A ttempts are under-way in other countries to fortify sugar withless expensive iron sources.Rice

Rice is a logical vehicle for iron fortifica-tion because it is a staple food for more thanhalf the world s population and the maincomponent of the diet in many countrieswhere nutritional anemia is highly preva-lent. Early studies using biosynthetically la-beled rice showed low absorption of its in-trinsic iron (43), but more recent measure-ments with an extrinsic tag have shown ab-

sorption to be comparable to other cerealsand grains (27). W here rice is the staple food,its intake is closely tied to caloric intake andvaries little with respect to income. I n someareas home milling may be a drawback withthis vehicle but in most countries it is milledcommercially. Government control of thefortification process would be difficult incountries such as the Philippines where thereis a large number of small mills.

T he usual approach to fortifying rice is toprepare a premix of rice grains coated withiron and other nutrients which is then mixedwith common rice in a ratio of 1:99-1:199(44, 45). A s with other food vehicles, thepoor masking property of rice poses a tech-nical problem because even a few discoloredgrains may make the product unacceptable.T his can be solved by using an inert form ofiron such as ferric orthophosphate or ferricphosphate but these iron sources are notlikely to improve iron status. I n a studyconducted in 1949 in Bataan, Philippines(44), fortified rice was said to reduce theprevalence of anemia, but efficacy has notbeen adequately evaluated. Rice fortificationhas been required by law in the Philippinessince 1 950 but this has never been enforced.

T he focus of recent studies has been tocoat rice with a more available form of ironsuch as ferrous sulfate and to mask colorchanges in the fortified grain with a coatingagent such as talc. One possible approach isto seal the iron with an edible polymer whichwould resist both washing and cooking andyet rapidly disintegrate in the intestinal tract(46). H owever, it is generally assumed thatthe enriched rice should be coated in a man-ncr that would minimize iron loss duringwashing but ensure complete release duringcooking. I n this case, cooking water andcluted iron must be reabsorbed by the ricegrain to minimize nutrient loss.W e have recently prepared a rice premixusing ferrous sulfate and an intermittentshellacking process (M orck T A , L ynch SR,Cook JD , unpublished observations). T hepremix was fortified to a level that wouldprovide 8 to 10 mg iron daily (3 mg iron/100 mg rice) at a 1 :99 dilution with commonrice. T he fortified grains were whitened withtalc and were barely detectable when mixedinto unfortified rice. T he iron coat was ne-sistant to washing in a conventional rinse


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654 CO OK A N D REU SSERtest but isotopic studies showed absorptionof less than 50 % as compared to iron inother foods eaten simultaneously, appar-ently because the iron was not fully releasedfrom the coated grain.

I n another preliminary study in the Phil-ippines, a rice premix designed for 1:200dilution with common rice was coated withsufficient ferrous sulfate to provide the fullrecommended daily allowance for iron (18mg), assuming a per capita intake of 300 graw rice daily (42). T his premix was coatedby dispersing anhydrous ferrous sulfate inan isopropyl-chloroform coating solutionand the suspension was mixed with raw ricein a rotary pan until the grains were uni-formly coated. T he premix was air dried atroom temperature for 1 h, then packed andstored in polyethylene bags. A lthough lessthan 10% of the added iron was lost duringrinsing, the iron content of the premix wasreduced by 25 % after 8 wk storage at roomtemperature and by over 50% after 8 wkaccelerated storage at 50#{176}C .eriodic sensoryevaluation of the enriched rice showed ac-ceptable results after 1 2 wk storage at roomtemperature but both the color and flavorwere affected by storage at 50#{176}C .hese re-cent observations suggest that the technicalproblems in coating rice with an availableform of iron are by no means insurmount-able.Condiments

Problems with color, taste, and odor of aniron fortified vehicle can be minimized byusing a highly flavored substance such asfish sauce or fish paste, condiments whichare used in place of salt in certain East A siancountries. Fish sauce is a colored, stronglyflavored extract of marine fish with a highsalt content. I n T hailand, fish sauce (nam-pla) is produced through fermentation byhundreds of small companies and soldthrough local stores and street vendors. M ostforms of iron are rapidly precipitated whenadded to this product but this has beencircumvented by using N aFeED T A whichdoes not cause storage problems or changesin appearance or taste and is not detectableby the consumer (2 1). I n a I 2-month fieldtrial using fish sauce fortified to a level of 1mg/ml, a good H b response was observed in

iron-deficient women and children (2 1). A n-other large field trial w ith this fortificationstrategy is in progress in T hailand. One con-straint to using fish sauce as an iron vehicleis that it is not used in all regions of thecountry although its consumption is pro-gr essi vcl y i ncr easi ng.

Fish-based condiments have also beenproposed as vehicles in the Philippineswhere there are two common products, fishsauce (patis) and fish paste (bagoong). T hesecondiments are prepared by mixing one partsalt to three parts fish or shrimp, packingthe mixture in wooden vats or concretetanks, and allowing it to ferment for 6 to 18months. Fish sauce is a clear, amber-coloredextract specified to contain no less than 10%protein and 25 % salt by weight. I t is a highquality product consumed only by the upperincome segments of the population. Fishpaste is a similar fermented product of lowerquality which is consumed by the majorityof individuals in the low socioeconomic seg-ment of the population. Fish paste could befortified by adding N aFeED T A directly orby using a highly fortified premix of fishsauce which is used to prime the fermenta-tion of fish paste.Maiz e

M aize has desirable properties as a vehiclefor iron but it is a staple food in relativelyfew areas of the world. Corn meal and corngrits have been fortified with iron in theU SA for many years (47) and present nomajor technical problems. W hen these dry-milled products were fortified to a level of40 mg iron/lb with reduced iron, little or nosegregation occurred and no adverse odorsor flavors were encountered after 56 days ofaccelerated storage (48). On the other hand,stabilized ferrous sulfate at this level causedsome deterioration in flavor and odor.M aize has not been evaluated as a primaryvehicle for iron in any developing country;one reason may be that the food is com-monly processed in the home in rural areas.M ilk produ cts

A ttention in this review has been given tovehicles that would be consumed by most ofthe population in a given geographic region.W hile this does not apply to milk products,


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I R ON FOR TI FI C A T I O N : U PD A T E 655

they arc considered here bccausc of theirpotential importance as vehicles for ironduring childhood, particularly the 1st yr oflife (49, 50) . T he infant s relatively generousendowment of iron at birth disappears rap-idly during the first few months as body sizeincreases. A lthough the iron content of hu-man milk is relatively low, it can meet ironrequirements through much of infancy (51-53); from the standpoint of iron nutrition,breast-feeding is strongly advised for at least6 months and preferably longer. I f breast-feeding is discontinued, sufficient iron canbe provided in infant formulas to preventthe development of iron deficiency. A bsorp-tion ofadded iron is comparable from cowsmilk, pasteurized milk, condensed milk,evaporated milk, reconstituted powder, andmilk-based formulas with added carbohy-drates and fat (54). A s a vehicle for iron,infant formula has the advantage that it canbe fortified with highly available iron sourcessuch as ferrous sulfate, ferrous gluconate, orferrous lactate. M oreover, because of thelimited amount of the vehicle that must befortified, ascorbic acid can be included toenhance bioavailability at reasonable cost.

Extensive work with fortified milk for-mulas has been conducted in Chile (49)where powdered milk is distributed by thegovernment to over 80% of infants and lac-tating mothers. A bout 3 kg milk powder isgiven monthly from birth to 6 months ofage and 2 kg from 6 to 12 months. M eanduration ofbreast-feeding is about 3 monthsand solids are introduced at about 4 monthsofage. I n an initial fortification trial, low fatmilk powder was fortified with ferrous sul-fate to provide 1 5 mg iron/l reconstitutedmilk. A lthough the prevalence of anemiawas reduced substantially when this fortifiedproduct was given from 3 to 1 5 months ofage, some of the milk was consumed byother family members and the amount ofabsorbed iron was too small to prevent irondeficiency in a significant proportion of theinfants. I n a subsequent trial, the productwas acidified to discourage family consump-tion and ascorbic acid (100 mg/l) was addedto facilitate absorption. T his fortified milkreduced the prevalence of anemia at 15months of age to less than 2% as comparedto 28% in infants receiving unfortified for-

mula. T hese findin& s clearly demonstratethe efficacy of infant formula as an ironvehicle.P rocessed cerea ls

I ron-fortified infant cereals can also satisfythe high growth requirements for iron after3 months of age and are suitable for use inthe breast-fed infant (54) . T he technicalproblems are similar to those encounteredwith flour. Ferrous sulfate is an unsuitableiron source because of its tendency to causerancidity with prolonged storage. H igh ironlevels can be achieved with less availableforms of iron such as ferric orthophosphateor sodium iron pyrophosphate but efficacyis a concern. T his has led to extensive use ofelemental iron powders ofsmall particle size,particularly electrolytic iron, for the fortifi-cation of proprietary dry cereals in N orthA merica. Bioavailability is believed to beadequate, but again there is a need for asimple method to monitor bioavailability ofthese iron forms.

Blended food supplements make up animportant subgroup of processed cereals.Corn-soy-milk which consists of 59% maizemeal, 1 7% soy flour, and 1 5% nonfat milk,and 5% soybean oil (27), is fortified with 16mg iron as ferrous fumarate and 40 mgascorbic acid/lOO g dry cereal, giving a mo-lar ratio of ascorbic acid:iron of about 0.7.A lthough the effect on iron status of thisparticular product has not been evaluated ina field setting, there is little doubt that if abioavailable form of iron is used and ade-quate amounts of ascorbic acid arc added(55), these foods w ould have a major impacton iron nutrition in the most vulnerablesegment of a population (27).Other

Several other food vehicles for iron havebeen proposed but these have not been ad-equately studied or cover only limited pop-ulation groups. Because of their excellentmasking properties, dried fish productsmight be suitable in fish-consuming popu-lations such as Southeast A sia. I n a recentstudy in Japan, 30 to 80 mg iron/day wasadded to the diet by fortifying boiled anddried anchovies (tsukudani) w ith ferrous sul-fate (56). N o technical problems were en-


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6 5 6 COOK A N D R EU S S ERcoun te red and som e im pro v em en t in hem o -g lo b in lev els w as ob se rv ed du ring a 3-m on thf ie ld trial . C urry m ix (m asala) has been pro -po sed as an iron v eh ic le in an Ind ian popu-latio n liv ing in D u rban , S ou th A f rica (57).A sign if ican t inc rease in ab sorbed iron oc -cu rred w hen th is prod uc t w as f ortif ied w ithN aFeEDT A , and th e v eh ic le has the add edad v an tage that it p rom o tes iron absorp tionev en w itho u t iro n , pre sum ab ly by s tim u lat-ing gas tric acid sec retion .

B ecause o f th e ex cep tio nally h igh absorp -tio n o f hem e iro n , d ried H b , w h ich is cx -tracted f rom slaugh te r h ou se b lo od , has beenpro po sed f or f o rtif ication . T h e m ost ad -v anced w ork in th is area has been conduc tedin C h ile w here ch oco late co ok ie s h av e beenprepared w ith 6% H b (58). T he se coo k ie sare pre sen tly d is tribu ted to 750 ,00 0 ch ild renas p art o f a sch oo l lun ch prog ram . E achch ild receiv e s 3 0 g o f coo k ie s daily w h ichcon tain 1 .8 g Hb o r 5 m g hem e iro n andpro v ide abou t 1 m g absorb ed iron daily . T h ep rog ram requ ire s 16 ton s o f dried H bm on th ly , o r abou t 12 5 ,0 00 1 ofw ho le b lo od ;the co s t o f th e pro gram is U S $0 .54 /ch ild /6 -m on th schoo l y ear. A gratif y ing im pro v e -m en t in H b lev e ls has b een obse rv ed in p ilo ts tudies .

T he o p tion s f o r f o rtif y in g com m erc iallyav ailab le f oo d p roduc ts in dev e lo ped coun -tries are n um ero us . In the U S A , a v arie ty o ff o od s such as dried break f as t ce reals an drecons ti tu ted b ev e rag es are f ort if ied w ithiro n and o f ten p rom oted com m erc ially onth is b as is . For ex am ple , so f t d rin k s h av ebeen p ropo sed as v eh ic le s (3 9 , 59 ) and th ereis cu rren tly a f ru it- f lav o red b ev e rag e m ar-k e ted in S co tland called Irn B ru that isf o rtif ied w ith f ern ic am m on ium c itrate .H ow ev er, th ere are leg itim ate co ncern s w ithth is haphaz ard app ro ach to iro n f orti f ica-tio n . It is v irtually im poss ib le to asce rtainth e e f f ec t o f an y o ne produc t on iron balancein the popu lation and it is d if f icu l t to regu -late th e lev el o f iro n supp lied to the popu -lation as a w ho le . T he m o st im po rtan t co n -cern is that ind iv id uals w ho hav e an in he r-ited d ef e ct in the ab ility to reg u late iro nabso rp tio n f rom the g as tro in tes tin al trac tm ay con sum e ex ce ssiv e am oun ts o f the f o r-tif ied p roduc t and th e reb y accele rate the rateo f tissue iro n load in g .

Fo rtif icat ion pro gram sW hile the se le ct ion o f th e f oo d v eh ic le

an d iron so urce are prim ary con sid e ratio ns ,the re are o the r asp ec ts to dev e lo p in g a f or-tif ication p rog ram . T he f u ll sequ en ce o f re -qu ired s teps is o u tl ined in T ab le 3 . Prev a-len ce s tud ies are need ed at the o u tse t toes tab lish th at iro n d ef ic iency is su f f ic ien tlyw ide spread to w arran t a n ation al in te rv en -tio n p rogram ; iron de f ic ien cy l im ited to cer-tam segm en ts o f a p opu latio n can b e dealtw ith m o re e f f ec tiv e ly by su pp lem en tatio n o rtarge ted f ortif icatio n . H av in g de term in edth e need f o r f o rtif icat ion , d ie tary su rv ey s arenece ssary to ch arac teriz e the reg ion al d ie tw ith resp ec t to its co n ten t o f hem e andnonh em e iron and f ac tors th at enh an ce o rin h ib it iron ab sorp tion . It is de s irab le tom easure iro n absorp tio n f rom the reg io nald ie t in h um an sub jec ts u sing the ex trin s icrad io iron tag m etho d . T he se d ie tary su rv ey sand iso to p ic stud ies are th e b as is fo r de te r-m in ing w h eth e r the m ajor prob lem is lim -i ted iro n in tak e , low b ioav ailab il ity , o r bo th ,an d f or es tim ating th e le v e l o f iro n f orti f i-catio n th at w ill be req u ired to redu ce th eprev alence o f iron d ef ic iency .

O ne o f th e m ore cos tly and tim e-con sum -ing s teps in d ev elop ing a nation al f o rtif ica-tio n po licy is co nduc tin g f ie ld trials to es tab -lish e f f icacy . T h e n eed f or a f ie ld trial is lessc ritical if rad io iro n m easu rem en ts are pen -f o rm ed w ith the reg ion al d ie t to m easu re theactu al inc rease in absorb ed iron th at re su ltsf rom f orti f icatio n . H ow ev e r, because a cen -tral issu e w ith f o rti f icatio n is i ts lon g -te rme f f ec tiv en ess , it is im portan t to te st th e pro -g ram und er f ie ld co nd itio ns .T A B L E 3D ev e lopm en t o f an iro nf ortif ic atio n s trate gy1 . Dete rm ine p rev alen ce o f iron d e f ic iency2 . D e te rm ine iron in tak e f rom d ie tary su rv ey3 . M easure basal iron absorp tion f rom ty p ical d ie t4 . O b tain con sum p tion d ata f o r po ten tial v eh ic le s5 . C hoo se ty pe and am oun t o f iron f o rtif ican t6 . D ev e lop f o rtif icatio n techno log y7 . Perf o rm sto rage stud ie s o f f o rtif ied v eh icle8 . Perf o rm iso top ic m easurem en ts to de te rm ine in -

c rem en t in abso rp tion9 . C on duc t f ie ld trial to de term in e e f f icacy

10 . Im p lem en t a national strategy w ith con tinued ev al-uation


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IR ON FO RT I FICA T IO N : U PD A T ET A BL E 4C auses of unsuccessful field trialsFortification level too lowL ow bioavailability of fortification ironI nhibitory effect of regional dietPoor consum er acceptanceD eficiencies in laboratory assessment of iron statusD uration oftrial too shortI nadequate study design or statistical evaluationL ow initial prevalence of iron deficiencyH eav y p ar asi ti smO ther causes of anemia

population after implementation ofthe pro-gram. H owever, there are many factors thatmay contribute to a change in iron status ina given country over time and without fieldtrials there can be no certainty as to theprecise impact of the fortification policy perSc. T he more costly the fortification programand the more limited the economic re-sources of the developing country, the moreimportant it is to avoid adopting a programof questionable benefit. C !

Field studies may fail to demonstrate abeneficial effect of fortification for a varietyof reasons (T able 4) . T he impact on ironstatus will obviously depend on the amountof added iron and the bioavailability of theiron source. I n addition, basal absorptionfrom the regional diet may be so low thatincreasing iron intake may have little effect.T he trial may prove ineffective because thefortified product is not widely consumed orwell accepted by the population. T here arealso pitfalls related to the design and conductof the trial itself. Preliminary hematologicalsurveys should always be performed in theregion proposed for the field trial to ensurethat there is in fact a high prevalence of irondeficiency. T he ability to detect smallchanges in iron nutrition in a population hasbeen greatly enhanced in recent years byusing a battery of iron status measurementssuch as transferrin saturation, red cell pro-toporphyrin, and serum ferritin (1 , 60, 61),but these must be carefully performed andadequately standardized. I t is necessary toconduct the trial for an adequate period oftime as iron status does not change rapidlywith fortification. A field trial may also failbecause of heavy parasitism or malabsorp-tion in the target population and iron willnot alleviate anemia due to other causes suchas chronic inf ection.

A field trial is expensive and can takeseveral years to design, conduct, and ana-lyze. I n countries where the cost ofa prelim-mary field trial is prohibitive or where thehigh prevalence of iron deficiency anemianecessitates immediate action, it would bereasonable to forego the trial and proceeddirectly to a national fortification program.I n this case the efficacy of fortification mustbe assessed by monitoring iron status in the

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iron fortification an update

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