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91 6 Th e Am er ican Journ a l o fC lin ica J N u tr itio n 32 : A PR IL 1979 , pp . 916-925. Prin ted in U .S .A .

Iron de fic iency anem ia and the p roduc tiv ityo f adu lt m a les in Indones ia1 2Sam ir S . B asta ,3 D . Sc ., So ek irm an ,4 M . S . , D arw in K aryad i,5 M .D .,a nd N ev in S . S cr im sh aw ,6 Ph .D ., M .D .

A B S T R A C T A pprox im ate ly 88 % o f adu lt m ale w orkers on a rubber p lan ta tion in W est Java ,In don esia had ho ok w orm in fection , an d ove r 45 % w ere an em ic a s ju dg ed by a he m o glo bin b elo w1 3 g/lO O m l. H em o glob in va lues and H arvard S tep T est (H S T ) p erfo rm ance for bo th tapp ers an d

w ee ders w ere s ign ific antly co rre late d . T he ru bbe r tap pe rs w ere p aid by th eir w ork ou tpu t, andthe i r earn in gs corre la ted w ith hem o glob in leve ls. M orb id ity and hem oglob in leve ls w ere a lsocorre la ted . C a lo ric in takes w ere n o t corre la ted w ith e ithe r w ork ou tpu t o r H S T perfo rm ance .T reatm ent w ith 10 0 m g of e lem ental iron for 60 d ay s resu lted in a sign ifican t im pro vem ent inh em ato log ica l sta tus o f th e an em ic ind iv idua ls and in the ir H ST pe rfo rm anc e, w ork ou tpu t, andmorb id i ty . B o th trea tm ent an d p lacebo group s rece ived a da ily in cen tive pay m en t of 15 ru p iah s,equ iva len t to 5 to 7% of m inim um da ily w age s. T his sum , spe nt larg ely on food , re sulted in a dd edin takes of 3 to S m g of ava ilab le iron and 50 m g of v itam in C . T his is be liev ed to ex p la in asig nifican t b ut le sse r im p rov em ent in hem og lob in , H ST p erform an ce, w o rk o utp ut, a nd m o rbid ityin th e anem ic p lacebo g roup . In an u n treated subsam p le to w ho m no paym ent w as giv en, n oc h a n g e in he m o glo bin , h em ato cri t, w ork perform a nce , H S T sco re, or d isease m orb id ity occurred .A fte r in co m e su pp lem entation w as s to pped , hem oglob in an d h em atocrit leve ls and re la ted chan gesrev er ted to in itia l leve ls w ith in 3 0 days in the p lacebo grou ps, bu t w ere unchanged in the iro n-trea ted gro ups . T he co st o f th e iron su pp lem enta tion w as sm all com pared w ith the econom icbenefits o f inc reased produ ctiv ity and lo wered m orbid ity . Am . I. C lin . N u ir. 32: 91 6-9 25 , 19 79 .

B ecau se an em ia d oes n o t h ave ov ert, spe -c ific sym ptom s and is d iag no sed b y labo ra -to ry p rocedu res , it is no t ord ina rily recog -n ized b y lay pe rso ns as a d isease . Its sym p-to m s a re sub tle , chro n ic , and asso cia ted w ithth ose of o the r d iseases . It can im p air ex e rc isepe r f or m ance 1 -5 an d is a po ten tia lly im -p ortan t de te rm inan t of labor pro du ctiv ity .

In the tro p ics , th e com bin ation of b lo odlo ss from p arasitic in fec tio n , e sp ec ia lly ho ok-w o rm (6 -8), and low av ailab ility of d ie ta ryiro n (9) is th e m o st co m m o n cau se o f ironde ficien cy anem ia. Iro n de ficien cy an em iaa ffec ts phy sical capacity b y red uc ing theava ilab ility of o xy gen to th e tissu es , w h ich , intu rn , a ffects ca rd iac o u tpu t and the h eart. Ita lso redu ces the e ffic ien cy of ox yg en cx-ch an ge in m u sc le an d m yo glo b in . E xpe ri-m enta l ev id en ce su gg ests th at suscep tib il ityto in fec tion m ay b e in creased because m ye lo -pe rox idase, an iro n-con ta in in g en zy m e th atp lays a v ita l ro le in th e k ill ing po w er ofleucocy te s , is a lso affec ted (1 0 , 1 1 ).

In a p ilo t labo r pro du ctiv ity s tud y in In -d on esia , an a ttem p t w as m ade to m easure the

e ffec t o f correcting th e iro n de ficien cy o f 10 0ro ad co nstru ction w o rke rs . B ecause o f theh igh dro po ut ra te s and the cessa tion of m an yw o rk activ it ies caused b y heav y m o nsoo nrain s , da ta w ere ob tained on on ly 2 2 iron-trea ted an d 2 0 placeb o-trea ted w o rke rs . T heresu lts , ho w ev er, ind icated tha t p hy sica l pe r-fo rm ance o f anem ic w o rke rs cou ld be im -pro ved b y adm in istration o f 10 0 m g o f d c-m ental iron d aily for 4 w eeks. P rod uc tiv itype r se w as not m easured , b u t on ly ph ysicalendu rance du ring th e H arv ard S tep T est(H S T ). T he stu dy ind icated a sign ifican t co r-relation am o ng h em og lo b in , h em atoc rit, an d

I F rom the N utrition R esearch Ins titu te , Sem bajaUn i t , B og or , I nd on es ia .

2 S u p p o rte d b y the R esearch D ivis ion , T ra nsp ortatio nand U rban P ro jects o fT he W orld B ank (IB R D ) w ith theactive in terest and he lp of D r. A nth on y C hu rch ill, D r .C le ll G . H a rral , an d M r. L e on M iller .

J N u trit ion Spe cia list , W o rld B a nk , W a shington ,D .C . T ea m L ead er, A c ade m y of N u trit ion , Jak arta ,Indon esia . D irec to r, N utritio n R esearch Institu te ,B og or , I nd on es ia . Ins titu te P rofessor a nd H ea d, D c-partm en t o f N utrition an d Foo d S cience , M assachu se ttsIns titu te of T ec hn olo gy, C am bridg e, M a ssa chu setts.

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IR O N D E F IC IE N C Y A N E M IA IN IN D O N E S IA 91 7H S T scores , a lth ou gh oth er n u trien t in takes ,inc lud in g tha t o f ca lo ries , d id n o t co rrelatew ith the H S T .

T h is ex pe rien ce p rov ided the basis fo r thecu rren t in te rven tion p rog ram am on g ru bb erp lan ta tio n w o rk e rs to d eterm ine : (1 ) whe the ranem ia in low -in co m e w o rke rs a ffec ted ph ys-ica l end urance, th eir ac tua l p ro du ctiv ity , andthe ir res is tance to in fec tio n , an d (2 ) whe the riron sup plem en ta tion co uld d im in ish iron de -fic iency an em ia and ra ise w o rk o utp u t in th ispopula t ion .M a te rials and m etho dsChara cte ris tics o f the pop u la tio n

A to ta l of 302 m ale p lan ta tion w orkers , 16 to 40 yearso ld , selec ted ran dom ly from a lis t o f 4 00 w orkers , w ered iv id ed in to anem ic (152) and nonanem ic (150 ) g roup so n th e b as is o f a hem atocrit b elow or above 38% . T hem ajority of the w ork ers w ere tapp ers w ho co llected la texfrom 40 0 to 50 0 rub ber tre es pe r da y, w h ile w ee de rs(abou t 3 0% of th e to ta l w ork fo rce ) w ere m ain ly resp on-s ib le fo r c lea ring and d igg in g ju ng le roo ts around theru bbe r tre es, com pletin g an ave rag e of 70 to 10 0 m 2 a reape r d ay.

S eve nty tap pe rs a nd 83 w ee ders rece ived 10 0 m g offe rrou s su lfa te in dex tro se da ily fo r a p er io d of 60 days ,w hile the c ontro l g rou p (8 6 ta ppe rs an d 63 w eeders) w ereg iven an iden tical look ing dex trose tab le t.7 N eith e r thew ork ers nor those ad m in isterin g the tablets kne w w how as rece iv ing the iron o r p lacebo . A lthoug h som e w ork -ers h ad d ark co lore d stools, th ey did no t kno w th es ig n ificance of th is , and by d es ign , no a tten tio n w as p aidto it.

To encourage partic ipa tion , a p aym ent of 15 ru p iahs(a pproxim a tely 3 U .S .) w as g ive n daily to w o rke rs inbo th gro ups w he n th e tab let w as tak en. N ev erth ele ss, 41ind iv idua ls d id d rop ou t o f the p rogram , an d an add i-tio na l 10 sub jects w e re e lim ina ted from th e fin al an aly sisbecause the y re ceiv ed o the r m e dic atio n th at m ight h avepre jud iced the resu lts . A subg roup , co nsis tin g of 5 1w o rkers , w ho rece ived no iron , p lacebo , o r incom e sup-plement, w as a lso tested hem ato log ica lly befo re and af tert he i nt er ve nt io n. edic al e xam in ation

Ex am in ations w ere co nduc ted b efore and im m ed i-a te ly a fter the in te rven tion s tudy , and the phys icianv is ited the s ite frequ en tly durin g the s tu dy . D iseasesrep orted by th e sub jec ts to h av e occurred in the 4 w eek sb efo re the f irs t ex am ination w ere reco rde d. These we r echarac te rized as acu te (e .g ., com m on co ld , in fluenza ,h ep a titis); subacu te (e .g ., a rth ritis ), o r ch ron ic (e .g ., tu -b ercu lo s is . T h ey w ere sco red o n a sca le of 0 to 3accord in g to severity and dura tion , and the fig ure s w e read ded to g ive a to ta l m orb id ity sc ore . In ad dit ion , g ene ralp hys ica l cond ition and nu tritio na l sta tus w e re sc ore d .A b sen ce fro m w ork fo r an y reason , inc lud ing tire d-ness, w as a lso recorded and sco red . H eigh t, w e igh t, andm id -arm circum ferenc e w ere a ls o r ec or de d fo r eac h su b-jec t. M ean h eigh t fo r th e sam ple w as 1 57 .4 5. 3 cm ,

an d m e a n w e igh t w a s 46 .9 4.9 k g. M ean ag e w as 29 .3 7 .5 y ea rs .La bo ra tory ex am ina tio ns

Hemato l ogy . Us in g pre ste rilized in div idu al d ispo sa blelance ts , f in ger-p rick b lood sam ples w ere tak en fo r de te r-m ina tio n of h em o glob in and hem ato cr it, and b lo odsm ears w ere m ade to de tec t m ala ria paras ites an d d efin ere d ce ll m orp hology . D up lic ate he par in iz ed m icro -he -m ato crit tub es w e re ce ntr ifug ed at 1 5 ,0 00 rp m for 5 m m .H em oglob in w as es tim ated as cyanom ethem og lo b in (12).

A 10 m l b lood sam ple w as draw n from all ind iv id ua lsw ith a h em ato cri t b elo w 38 and p ut in to a h epa rin ize dvacu ta iner tube for de te rm ina tion o f o th er b lood char-acte r i s t i cs . Serum iro n w as m ea sured by the W orldH ealth O rg anization m eth od o f pla sm a-iron de term in a-tion , a m od if ica tion ofthe techn ique or ig in a lly desc ribedby B o th w ell and M alle t (13 ). T o ta l iron-b ind ing cap acity(TIB C ) w as tes ted by a m eth od diffe ring sl igh tly fro mtha t o rig ina lly desc rib ed by R am say (14); tha t is, su lfon-a ted ba thop henan th ro line w as u sed fo r co lo rim etric de-te rm ina tion . B loo d film w a s sta ine d w ith G iem sa solu -t io n fo r d iffe ren tia l w hite b lood ce ll co un t and exam inedm ic roscop ica lly for ab no rm a lities in c ell m orp hologyre la ted to defic iency d isease , acco rd ing to th e m ethodre co m m end ed b y W orld H ealth O rg an izat ion /Pa nA m erican H ea lth O rgan iza tio n (15 ).

A 20 % subsamp le , ch ose n at rand om fro m the iro n-p a y m e n t a nd pla ceb o-p aym en t group s, w as reex am ine dafter in terv ention for serum iron, tra nsfe rrin , and T IB Cleve ls. H em oglob in an d hem atocrit w ere assessed no ton ly 6 0 da ys a fte r in terv en tion in the entire g rou p, bu ta lso at 91 an d 10 0 da ys po stin terven tio n in 7 1 su bje ctsch osen from the above . A s a furthe r con tro l, the S iu ntreated indiv id uals w ere reex am ine d for hem ato cri tan d hem o glo bin after th e in te rve ntio n p erio d .

Paras i t o l ogy . F eca l sam ples w ere o b ta in ed from 10%of the w o rke rs. Im m edia tely af ter c olle ction , ap proxi-mat ely 2 g of the sam ple w ere transfe rred to a 2 -ouncebo ttle w ith scre w top an d tho rou gh ly m ixed w ith a nequa l am ount o f 1% fo rm alin fo r la te r lab ora to ry cx -am in a tion . M icroscop ic exam ina tio n for the presence ofparasites and eggs, and S to ll coun ts (1 6) fo r egg concen-tra tion s of sam ples p ositive for hoo kw orm , w ere c arriedou t by the D e pa rtm ent o f P ara sito lo gy, Fa culty of M c d-icine, U niv ers ity o f In do nes ia .Dietary interv iews

T he die tary da ta w e re collected by a trained n utri-tionist f rom a 2 5% sub sam ple, us ing a com bination oftechn iques from B urke (1 7), K le rk s ( 18 ), and . th e D irec -torate of N utritio n of Ind onesia . Each respo nden t de-sc r ibed th e kinds of food ea ten and the freq uency ofea tin g dur in g the prev ious w eek s. D etailed qu es tionsthen gave an aprox im ate am oun t of the foods consum edm o s t f requently . Fo od item s pu rchased fro m lo ca l foodse llers w e re use d as m o dels, in add itio n to pic tures offoods . Ra w and cook ed foods w ere w eighe d, a nd th eirnu trien t con ten t calcula ted fro m the Ind one sia n FoodC om position T ab le (1 9). B ecause the m enu s w ere m ostly

7 T h e sacc har ine an d ta pio ca pla ceb o a nd the fe rro ussu lfate tab lets w ere supp lie d by K im ia Fa rm a , S .A .,Jakar ta .

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91 8 B A S T A E T A L .s imp le an d m o no ton ous , the d ieta ry in ta ke d ata w erequ i te rel iab le.

D ietary in terv ie w s o f sub jec ts after the inco m e su p-p lem en t h ad b een pro v ided ind ica ted tha t th is w aslargely spen t on var iou s e dib le lea ves , as rice w as ra -tio ne d. T he in cre ase d in ta ke of 20 0 g of green leaves p erw orker p ro v id ed an es tim ated 50 m g of ascorb ic ac idan d ab ou t 8 to 10 m g o f iro n , w ith the av ailab ility of thela tte r increas ing w ith the deg ree of an em ia in th e a p-p rox im ate range of 25 to 5 0% un der th ese c irc um stan ces .T h u s , the incom e sup p lem en t resu lted in an add ed 3 to5 m g of av ailab le iro n .

Ph ys ica lJItn es s a nd work c ap aci tyThe H ST , as a sim ple te st o f p hy sica l ca pa city , w as

p erfo rm ed b oth before and afte r the in te rven tion s tudy .Th e procedu re , eva lua tion , an d in terp re tation fo llow edth e orig in al m e tho d of B rou ha et al. (20 ), ex ce pt fo r th eb en ch h eigh t. D han u tir to and cow orkers (21 , 22) co rn-pared th ree benche s o f d iffe re n t he igh ts and concludedthat a 19-inch bench h eigh t ra the r than 2 0 in ches w asthe m o st su ita b le for Indo nes ian s.P ro du ct iv ity m ea su rem en ts

T o m easure w ork o u tpu t befo re and afte r in terven-t ion , tw o s tand ard tasks w ere se lec ted : the co lle ctio n ofw et late x by tap pe rs an d the w e eding or exc av atio n ofro o ts and w eeds be tw een the row s of rubb er trees . T ap-p ers w ere pa id d aily on the b asis o f th e w eigh t o f la texea ch m an de live red to w eig hin g hu ts. E ac h tapp erw o rke d 40 0 to 50 0 tree s, and th e d istanc e b etw ee n thet rees w as abou t 4 to 5 m . T he ou tpu t fo r w eeders w asm easured by th e area of trenches d ug in p aralle l row s b yeach m a n .Pas t reco rds o f paym ents to la tex tappers prov id ed au sefu l check on the incom e record ed during th e in te r-ven tio n program a nd f ur ni sh ed ano ther ind ex of produc-t iv ity . T he top ography , age , size , an d v ar ie ty of the treesw ere tak en in to acc ou nt by an aly zin g on ly d ata f romsim ilar tree areas . W o rke rs en gag ed in w e ed ing w erepa id on a da ily w age basis , w hich m ade p roduc tiv itym easurem ents m ore d ifficu lt. H ow ever, to ta l a rea exca-vated d urin g the 5-h r w o rk d ay w a s m e asu red for eac hin d iv id u a l. In ad d ition f in a n cia l in ce n tive s w er e o ffe re dto th ose m en w ho , in co m p eti tiv e g rou ps of 10, co uldw eed the larg est are a in 1 h r. T he pu rpo se w as to m easu rethe w eed ing capac ity of these ind iv id ua ls un der a s trongin cen tive . It w a s im possib le to ex ten d th e ra ces be yo nd1 hr b eca use m a ny o f the w orkers w ere nea r ex ha ustion .E ach gro up of 10 w as m atch ed for ag e, h eigh t, andex per ien ce. T he w in nin g group rec eiv ed th e eq uiv ale ntof 100% of the d aily w age , w ith run ners-u p rece iv ingd ecre asing po rtions o f th at su m .

Q uality con tro l w as establish ed by fore m e n w h o in -sp ected each area to be m easured . W eed ers w ere w arnedtha t if qua lity w a s not m a intain ed th ey co uld not c on-tinue in the com petition . M easurem ents on 61 w eederswe r e a lso con duc ted w hen they w ere no t w ork ing un derthese finan cia l in cen tives , an d w ere unaw are tha t the iro utp ut w as b ein g m easure d . T h is w ork perform an ce w ascom pa red w ith hem og lob in lev els a nd H S T perform an ceby linea r regression ana ly sis to d ete rm ine the re la tiv ein fluence of in te rv en tio n and other fac tors.

Co rre la t ion o f r esu ltsD ata w ere ana lyzed sta tistically using IB M 11 30 and

UN IVAC 1 1 08 com pu te rs . S ig n ifican ce o f the d iffe r-en c es b e tw ee n m ean s w as assessed b y S tu de nts t testan d ANOVA.

P rein te rven tio n c lin ica l resu ltsD ie ta ry in ta ke

T h e m ain so urce o f bo th ca lorie s an d pro -te in fo r p lan tation w ork ers is rice . C assav a,cocon ut o il , sug a r, an d tub ers p rov ide m o sto f th e res t o f the ir ca lo rie s . T he m a jority o fw ork ers con sum e accep tab le to h igh lev e ls ofv itam in C an d A from th e fru its an d ed ib leleaves tha t a re abu ndan t in the ju ng le. C al-ciu m , p ro te in , an d vitam in B in tak es a re lo w .

A nem ic w orke rs ave raged 20 00 198 .7ca l/d ay , 2 9 .9 2 .8 g /day p ro te in , 6 .2 0 .8m g /day iro n , and 6 0 .4 20 .6 m g/day v i-tam in C . N on an em ic w o rk e rs co nsu m ed 2 155 20 2 .8 cal/day , 3 1 .9 4 .2 g /day pro te in ,7. 4 1 .2 m g/d ay iron , and 10 0 .7 2 8 .2 m gIday vitam in C . T h ese d iffe rences b etw eenan em ic an d n on an em ic su b jec ts in th is s tud yw ere statist ica lly s ig n ifican t (P < 0 .0 1) forv itam in C on ly . T he ave rag e in take o f ironfor a ll th e w ork ers fe ll in the d efic ien t to lo wr ange .Labo ra to ryfin d ing s a nd clin ica l s ta tu s

T h e preva lence of an em ia , d efm ed as ahem o glob in be low 1 3 g /lO O m l, in th e en tiresam ple o f 3 99 w as 4 5 .4% ; 6 .3% of the sam p lehad hem o glob in leve ls b elow 1 1 g / 1 00 m l(T ab le 1 ), an d 25 o f th e hem ato crit va lu esw ere le ss th an 38 % . A bo ut 3 0% of an em icw ork ers had seru m iro n lev e ls be low 50 g /d l, and T IB C w as de ficien t in 65 .6% . H yp er-seg m en ted granu locy te s com b ined w ith ov alm ac rocy te s , sug gestive of fo la te o r B 1 2 de fi-c ien cy , w ere pre sen t in ab ou t 1 2% o f theanem ic m en.

In the 1 0% subsam ple of 1 62 w o rke rs se -lec ted fo r s too l exam in a tion , h oo kw orm eg gsw ere iden tified in 87 .7 % . A re la tio nsh ip w asfo un d be tw een the sev erity of th e in fe s tationan d hem ato c rit-hem o glob in lev els (T ab le 2 ).A scaris lum br ico ide s w ere rep orted in 48 .8 % ;T rich uris in 63 .4 % ; E scherich ia h is to ly tica in8 . 6 % ; E scherich ia co il in 1 2 .3 % ; and G iard ialambi la in 4 .3 % .

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IR O N D E F IC IE N C Y A N E M IA IN IN D O N E S IA 91 9

a C lass ifica tion accord in g to Prof. S ri O em iya ti, H ead , D epartm en t o f P arasito log y , U nivers ity ofInd on esia . M ean . C SD .

A b ou t 1% of the sam p le h ad sym pto m s o fv itam in A d efic iency , an d abo ut 2 2% ap-pea red g rossly un de rno urish ed .In fe ctio us d isease m o rb id ity

A b ou t 8 % of the p lan tation w o rke rs su f-fe red from system ic or loca l in fection d urin gth e 4 w eeks p reced in g the exam in a tion . P c-rio d preva lence w as alm o st tw ice as h igh inanem ic m en as it w as in the no n-anem ic. F orexam p le , the ratio w as ab ou t 8 :5 fo r in fluenzaand n ea rly 3 : 1 fo r b ronch itis . A nem ic m ena lso h ad on e -th ird m ore cases o f d ia rrhea.T h ere fore , in fec tiou s d isease m o rb id ity score sfo r the 1 81 in the anem ic g rou p (1 .6 3) w eresig n ifican tly h ig he r (P < 0 .01 ) than for th e2 21 in the n on an em ic gro up (1 .0 2). In ad d i-tion , th e re w as a sig n ifican t co rre la tio n (P