Am J Clin Nutr 1978 Cummings S21 9

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    T he m er ica n J ou rna l o f C lin ica l N u tr itio n 31 : O TO ER 1978 , pp . S 2l-S2 9 . P rin ted in U .S .A . S2 1

    Nu tr itio na l im p lica tio ns o f d ie ta ry fib e rJ o h n H C u m m in g s 2 M S c M B M R C P

    A BSTR A CT W hen dieta ry f ibe r in take s are increased b y su pplem enting d iets w ith b ran an dwhole w heat p rod uc ts, then feca l fa t, n itrogen , en erg y , an d m ineral e xc retion ris e . T hese change ssugg es t th at fibe r m ay be alte ring no rm al d ig est ive and ab sorp tiv e fu nction . R ecen t stu d ie s havecon firm ed th is and have also shown th at fib er o f d ifferen t com po sition and from con tra stin gsources pro du ces d if feren t phy sio log ica l ef fects. T he g el-fo rm in g poly sac cha ride s su ch as gua r gumand pectin a lte r th e pat tern of g luco se ab sorp tio n and are h ypo ch oles tero lem ic : fiber f rom cerealsis no t hy pocho lestero lem ic b ut ex erts a p ron ounced e ffec t o n the la rge gu t. D ie tary f ibe r is larg elyd ig este d in the co lo n b y the m icro flo ra and so in flu enc es co lo n ic fu nction , fe cal w eig h t. an dcom po sit ion . Th e s ign ific an ce o f the ch ang es in fa t, n itrogen , and energy o utp u t rem ain s to b eeva lua ted , bu t the im pa irm ent o f m in era l ab so rp tion-par ticu lar ly of calc ium , zinc, and iron -byf ibe r g iv es cause for co ncern . F ibe r m u st n ow be co nsidered w ith o th er d ieta ry co nst itu en ts in allnu tritiona l stu d ie s. m J C lin Nu t r 31: S 2l-S 29 , 19 78 .

    In add itio n to the inc rea sing ly w e ll-d ocu-m en ted e ffects f ibe r has on co lon ic fun ctio n ,it is now c lea r th at f ibe r is a nu trien t o fim portance in its ow n rig h t. T he am oun t an dty pe of fib er in clu ded in th e d ie t m ay h avesign if ican t n u tr itiona l im p licatio ns. T ab le Ilis ts the a rea s in w hich pub lished ev idencesugg ests th at fib er a lte rs the d igestio n ab so rp -tio n o r su bsequ en t m e tabo lism of va riousnu tr ien ts . A t the p resen t tim e, o ne w ou ld beu nw ise to stud y the n u tritio na l con seq uenceso f any g ro up o f sub stances in the d iet w ithou tin clu d ing som e refe rence to the ir in te rac tionw ith d ie tary f ibe r . W ith th e w e ll-p ub lic izedsug gestion tha t fib er de ficiency is a m a jo rp ub lic h ea lth p rob lem , expans ion o f resea rchin th is fie ld is in ev itab le. It is the re fo re im -p ortan t to e stab lish c lear p rio r ities . A lthou ghit is rela tive ly easy to show tha t f ibe r h as ane ffec t o n a pa rticu la r a sp ec t o f nu tr ition andnu tr ien t m etabo lism , it is m ore d iff icu lt andm ore im portan t to m easu re the sig n if icanceo f these ch an ges, p a rticu la rly in the lo ngt e rm .

    T rad ition al co ncep ts o f n u tr ition a re o f noh elp in consid era tions o n the ro le o f d ie ta ryfibe r . F ibe r can no t b e te rm ed an essen tia lnu tr ien t, an d it is no t ea sy to asce rta in m ansda ily requ irem en t fo r so va ried a sub stan ceas fib er . S tu d ie s w ith e lem en tal d ie ts d em -on stra te tha t m an can h iv e satisfacto rily fo r 6m on th s on a fibe r-free d iet 1 , the o n ly no -tab le ch an ge be ing a d ecrease in sto o l b u lka nd freq ue nc y.

    W he the r a long -te rm requ irem en t ex ists fo rf ibe r in m an rem a ins to b e answ ered .

    FatF ib er a lte rs lip id abso rp tion . W hen w ho le

    w hea t p ro duc ts such as b ran a re fed , feca l fa tex c re tion rise s . F ig u re 1 sh ow s fecal fatty ac idexc retio n m easu red b y gas liqu id ch rom a to g-rap hy in six m ed ical s tud en ts d u ring the 3 rdw eek o f a m e tab o lic s tudy in w hich th ey a teeith er a co n tro lled d ie t o r a d ie t to w hichw ho le w heat p rodu cts w ere added 2 . F ib erin tak e on the con tro lled d ie t w as 17 g /d ayand w as inc rea sed to 4 5 g /day b y ex chang in gw hite fo r w ho lem ea l b read and A ll B ran fo rco rn flakes, and by ad d ing a b ran b iscu it and3 0 g of b ran . A sm a ll chang e in fatty ac idin tak e from 86 to 9 6 g /day occurred , bu tfeca l fa tty ac id ou tpu t in creased sign if ican tlyfrom 1 .7 to 2 .7 g /day . F at exc retio n m easu redby the V an d e K am er techn ique 3 ro se from3 to 4 .5 g /day w ith the add itio na l fibe r .

    T h is inc rea se in fecah fa t is no t o ne th atw ou ld be consid ered sign ifican t in te rm s ofo ve ra ll d ig es tib ility and abso rp tion of fat, n o rd oes it rep re sen t a p ath o log ica l ris e in fecahfat ex cre tion in g as troen teroho g icah te rm s. Itis , how eve r, a w e ll-d escr ibed phenom enon .

    F rom th e M RC D unn N utrition L abora to ry , M iltonR oad , C am br idg e CB 4 1X J , Eng lan d .

    M em be r o f sc ien tific sta ff, D unn N utri tio n L abora -to ry an d hono rary co nsu lta n t p hy sic ian , A dd enb roo kesH os pita l, C am bridg e.

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    Su gg est ed n ut ri ti on alimplications

    Relevantb ib l iography

    Shor t-term requi rements for (1)f iber

    L ong- term def i ciency states W idely suggested butas yet unproven

    Ef fect on grow th U nknow n for manA bsorpt ion and metabol i sm

    Carbohydrate (17-27)Protein (2, 4-6, 9, 12)L ipid (2, 4-8)

    E f f ect on appeti te, sat iety , See other papers in thi sand obesi ty sy mposi um

    B i le acid and cholesterol me- See other papers i n thi stabol i sm sy mposi um

    V i tam i ns (39-44)M i neral absorpt i on

    Calcium (45-62)Iron (73-77)Z i nc (47, 63-72)

    parti cularl y about the ef f ect of f i ber f romcomm only eaten f rui ts and v egetables.

    A t the m oment w e can tentati v el y conchudethat the ov eral l balance of f at absorpti on isnot ser iousl y al tered by f iber but that sm al li ntesti nal ev ents leading to l i pid absorpti onare af fected. I n addi ti on, some f atty acidsm ay be associated w i th f i ber in such a w ay asto lead to thei r m alabsorpti on.

    A n increase in ni trogen as w el l as f at ex-creti on occurs w hen w hole w heat productsare fed (Fig. 2) (2, 4-6). T his increase in fecalni trogen is readi l y detectable but not nutri -ti onal l y signi f i cant in W estern industr i al i zedcomm uni ti es w here high protein intakes areusual . I t may of course be more important insocieti es such as those in rural A f ri ca w heredietary f i ber intakes are considerably higher.

    T he source of this fecal ni trogen remainsto be establ i shed. T w o suggestions are that i trepresents ei ther an increase in endogenousni trogen excreti on (5, 6) or i s due to thepresence of unav ai l able protein complex es (9)that pass through the gut undigested. T hesecomplexes are f orm ed during cook ing orother pretreatment of food bef ore eating andresul t f rom the degradation, condensation,

    DIET

    3

    2

    ME AN 1 7 2 7FIG . I . Fecal f atty aci d excretion in g/day (m ea-

    sured by gas l i qui d chrom atography ) i n six m edi calstudents during the 3rd w eek of m etabol i c diets of stan-dard W estern ty pe food or the sam e diet w i th w holem eal bread, A l l -B ran, and bran biscui ts (2).

    C O NT R O L 8 6 F IB R E 9 6

    M cCance and G laser (4) and M cCance andW alsham (5) noted fat absorpti on to be be-tw een only 54 and 62% complete f rom variousvarieti es of w hole w heat bread and onlysl i ghtl y greater f rom oatm eal . T hese f iguresare w el l below norm al fat absorpti on coef f i -cients observed w hen tradi ti onal W esternsty le food is eaten.

    D oes thi s change represent a true al terati onin the digesti ve and absorpti v e processes forfat i n the gut? O r i s a proporti on of the fatassociated w i th f i ber in such a w ay as to beunav ai l able for digestion? A l ternati v el y , doesthi s represent an increase in endogenousl i pid excreti on as suggested by W alker (6)?D etai l ed analyses of the f ecal f atty acids inour studies have suggested that at l east partof the f ecal fat consti tutes fatty acids associ -ated w i th f i ber in such a w ay that these acidspass through the gut undigested (H . S. W ig-gins, personal communication). K ay andT rusw el l (7) have show n that 15 g/day ofpectin can double f ecal fat ex creti on, andJenk ins et ah. (8) have show n guar gum alsoincreases fecal fat al though both the pectinand guar as f ed are l i pid f ree. T his suggeststhat the actual process of l i pid absorpti on canbe al tered in some w ay by f iber al though themechanism remains unclear. Few studieshave been done that throw much l ight on thi sf i nding, especial l y ones in w hich f iber otherthan that f rom w hole w heat or cereal prod-ucts i s used. M ore information i s needed

    S22 CU M M IN GS

    T A B L E 1N utri t i onal i mpl i cations of f i ber i nm an w ith selected bibl iography

    Nitrogen

    F A E C A LFAT T YAC I DS

    9 d a y

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    1-25 201

    N U T RI T IO N A L IM PL ICA T I ON S O F D IET A RY FIB ER S23

    D IE TA R Y N C O N T R O L 1 3 6 F IB R E 1 5 l

    2F A E C A LN I T R OGE N

    9 d a y

    M E AN

    1

    FI G. 2. Fecal ni trogen excretion i n g/day f rom samesubj ects as in Figure 1.

    and polym eri zati on of carbohy drates andam ino acids (10). V an Soest (11) has sug-gested that up to a thi rd of the total proteinin some break f ast cereals may be bound upin these complexes. T hey are know n as M ai l -hard complexes and interf ere w i th hignin m ea-surement.

    Fiber may also interf ere w i th the normaldigesti ve and absorpti ve pathw ays of protein.I t has recentl y been reported that in v i troacti v i ty of trypsin and chy motrypsin can beinhibi ted by v ar ious plant f i bers (12).

    A f urther possible explanation f or in-creased fecal ni trogen excreti on i s that i t rep-resents an increase in fecah m icrobial f l ora.A l though experiments using caref ul quanti -tati on of f ecal m icrobial f l ora w i th high-f i berdiets have so f ar fai l ed to show signi f i cantchanges in the f lora (13-16), the preci sion ofthe techniques used in these studies does notrule out the possibi l i ty of i ncreased numbersof m icrof l ora in the feces of f i ber-supple-m ented diets.Carbohydrate

    I t m ust have come as a surpri se to m anypeople in 1972 to f i nd T row el suggesting thatdiabetes w as a disorder related to our f i ber-def i cient diet (17); how ever, the relati v el y lowfasti ng blood sugar levels in rural A f r i canpeoples (18) and the rari ty of thi s condi ti onin com muni ti es consum ing high-f i ber dietshav e led sev eral people to take thi s suggestionseriousl y . I t i s now clear that dietary f i ber can

    al ter the process of carbohydrate absorpti onin man. Jenk ins et ah. (19) have show n thatadding 14.5 g of guar gum to a l i quid testm eal containing glucose or 10 g of pectin toa sol i d test meal containing bread, butter,m armalade, m i l k , and tea, or a com binationof these substances, leads to a signi f i cantf l attening of the blood glucose response tothese test m eals and that thi s i s accompaniedby a signi f i cant low ering of serum insul i nlev els measured sim ul taneously . A sim i lar butless str i k ing change in blood glucose af ter atest m eal containing bran w as show n by Jef -f reys (20), w hi l e bagasse and w ood cel l ulosetended i f any thing to have the opposi te ef f ect.T his w ork has been ex tended by Jenk ins eta . (21) to diabeti c subjects. T he response inblood glucose to a sol i d test meal containingboth 10 g of pectin and 16 g of guar gum w asconsiderably reduced in both insul i n-depend-ent and noninsuhin-dependent diabeti cs; sim -i l ar changes in the serum insul i n responsesw ere observ ed in the hatter group.

    T hese exper im ental changes are upheldw hen diabeti cs are f ed diets containing in-creased am ounts of dietary f i ber (22, 23).A l though in these dietary studies the intakesof f at, protein, and carbohydrate have al lbeen al tered in addi ti on to the change in f i berintake, i t i s clear that insul i n requi rementscan be reduced and f luctuations in bloodglucose m inim ized by these regimens. T heproblem of the etiology of diabetes remains,but thi s w ork prov ides a rati onal basis for anal ternati ve form of treatment.

    T he w ay in w hich these changes in glucoseabsorpti on are brought about remains to beestabl i shed. Jenk ins et a . (19) have suggestedseveral w ay s thi s could occur. Fi rst, glucoseabsorpti on rates could be al tered through thegel - form ing properti es of the w ater-solublef racti ons of f i ber al ter i ng the rate of di f f usionof glucose in the upper smal l i ntesti ne. G lu-cose absorpti on w ould, therefore, be show erand w ould be spread out along a greaterlength of intesti ne, thus enabl i ng ti ssue up-tak e to keep pace w i th absorpti on af ter ini ti alstim ulati on of insul i n release. T hese authors(19) dem onstrated no increase in the ev olu-ti on of breath hydrogen der i ved f rom thecolon so that ov eral l glucose mahabsorpti ondoes not occur. Second, f i ber may ef f ect therelease of gastrointesti nal horm ones andmodi f y pancreati c secretory and digesti v e

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    S24 CU M M I N G S

    processes. A l ternati vel y , changes may occurin gastri c empty ing or in sm al l i ntesti ne tran-si t time. M outh-to-cecum transi t time, asjudged by the evoluti on of breath hy drogen,may be delayed by these f orms of f i ber (24).T he l i kel y m echanism probably relates tolocal i nteracti ons of these v ar ious foodstuf f sin the sm al l i ntesti ne rather than to long-termchanges in the body s m etabol i c response toa glucose load al though the ev idence is some-w hat conf l i cting on thi s point (25-27). W hat-ev er the mechanism , how ev er, the observ a-ti on that carbohydrate absorpti on i s al teredby f iber remains a val i d one.

    F ib er d igest ionI n a considerati on of the nutr i ti onal impl i -

    cati ons of dietary f i ber, i t i s important toremember not only that f i ber af fects the ab-sorpti on of other nutr i ents but al so that i t i si tsel f digested in the human gut. Problem sw i th m ethodology hav e considerablyhindered research in thi s f i eld, but digestionof f i ber has been show n f rom sev eral sourcesincluding bran (28), m ixed diets (29), assortedvegetables (30), cel l ulose (31), and possibl ypectin (32). Southgate (33) pointed out thathum an capaci ty to digest f i ber v ar ies w idely ,but in general at l east hal f the f i ber i s digestedin the gut, most probably by the colonicm icrof l ora. T he breakdow n products of f i berinclude short-chain f atty acids, hydrogen,methane, and carbon diox ide.

    T he impl i cati ons of thi s are clearl y im por-tant and as yet incompletel y understood. O nekey aspect that has receiv ed some attention i sthe role of f i ber in fecal bulk ing. W i th ev i -dence now accumulati ng that short-chainfatty acids are absorbed f rom the hum anlarge bow el (34, 35) as they are f rom theanim al colon, i t seems l i kel y that the abi l i tyof a particular f i ber to resi st digesti on w ouldbe closely related to i ts f ecal bulk ing capaci ty .O ther im portant al terati ons in colonic phy si -ology are also l i kel y to occur.

    T he f actors control l i ng the break dow n off i ber in the hum an large bow el are uninves-ti gated, but, i f any paral l el s can be draw nw i th the nonrum inant animal , the composi -ti on of the f iber, i ts degree of higni f i cati on,mean transi t time through the gut, and theintesti nal m icrof l ora are al l l i k el y to be im-portant (36-38).

    V i t am i n sFew investigators hav e turned thei r atten-

    ti on to the possible ef f ect of f i ber on v i tam inmetabol i sm and absorpti on in the gut. W i ththe know n capaci ty of f i ber to adsorb organiccom pounds and the general associati on ofmalnutr i ti on and v i tam in def i ciency w i th sta-ple diets containing large amounts of f i ber,thi s seems a reasonable area f or research. I nv i tro studies have show n that v egetabhe ma-terial i s able to adsorb fol i c acid and i tsmonoglutamates (39), but no impai rment offol i c absorpti on f rom f iber-r i ch cereal prod-ucts occurs w hen f ed in test m eals to man(40). I ndeed i t w ould appear that high-f i berdiets stimulate intesti nal m icrobial synthesisof som e B v i tam ins (41, 42). R ats f ed veryhigh supplements of pectin or cel l ulose hav ebeen show n to have im pai red v i tam in B 12absorpti on, but i t i s doubtful i f these sort ofstudies w i l l hav e many paral l el s for m an (43).Investigati ons of the interacti ons of f i ber w i thv i tam ins i s partl y compl i cated by the pres-ence of signi f i cant quanti ti es of B v i tam insbound w i thin w hole w heat products (44).M in er al a bso r pt io nCalcium

    I t has long been know n that subjects f ed ahigh proporti on of w hole w heat products gointo negati ve calcium balance. Figure 3 show sthe calcium balance data for f our m edicalstudents doing a metabol i c study in w hich w ew ere reex am ining thi s question. I ni ti al l y adiet containing 88 g of f at, 13 g of protein,396 g of carbohydrate, 960 mg of calcium ,and 22 g of dietary f i ber w as f ed. Fiber intak ew as then increased by substi tuting 200 g ofw holem eal bread for w hi te bread, 25 g of A lB ran for cornf l akes, and 50 g of bran biscui tsfor N ice biscui ts, and adding 30 g of A hhinsonsB ran Plus. T hese addi ti ons increased dietaryf i ber intak e to 53 g/day , and, as a resul t ofcal cium hav ing been added to the biscui ts,cal cium intake increased to 1302 mg/day .D espi te the increase in calcium intake, thesubjects al l w ent into negati ve calcium bal -ance dur ing the 3rd w eek of the diet per iod.

    T his observation w as prev iously noted andstudied in some depth 30 years ago byM cCance, W iddow son, and others (5, 4 5, 46)and more recentl y by Rheinhold et al . (47,

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    N U T RIT I ON A L IM PL IC A T IO N S OF D IET A RY FI B ER S25

    FIG. 3. Cal cium balances in four medical students duri ng the 3rd w eek of m etabol i c diets. e ft c olum n f or eachsubject show s fecal and urinary calcium excretion in m g/day duri ng control W estern type diet. ig ht c o lum n f or eachsubject show s calcium ex cretion during the same diet i n w hi ch w hole w heat f oods had been substi tuted for equivalentref ined foods. Calci um ex cretion above the balance l ine represents negativ e calcium balance.

    48). T hei r w ork perhaps more than any otherev idence has cast doubt on the value ofw holem eal bread in our diet and has beenci ted as one of the f ew possible hazards toincreasing dietary f i ber intake f rom w holegrain sources. I t has even been suggested thatw hole w heat products may be responsible f orthe dev elopment of osteom alacia (49), andrecentl y these foods have been impl i cated inthe developm ent of ri ckets in chuppati -eatingim migrants in B ri tain 50 , 5 ).

    T he associati on of calcium malabsorpti onw i th w holegrain products i s tradi ti onal l y as-cribed to the phy ti c acid content of thesefoods (52, 53). W hi le i t i s undoubtedly truethat phy ti c acid im pai rs calcium absorpti on(46, 47), i t now seem s disti nctl y possible thatf i ber i tsel f may also hav e a role. Some of thequesti ons w e need to answ er in relati on tof i ber and m ineral balance are these:

    1) I s o ver al l balance af fected by f iber, or i schange one in route of ex creti on?

    2 ) Can changes be induced by commonlyeaten f iber sources and i f so at w hat lev els ofintake?

    3) W hich component of f i ber i s responsiblef or the changes in absorpti on (e.g., cel l ulose,l i gnin, noncel l ulosi c poly sacchar ides, or othercel l w al l consti tuents), and w hat are them echani sm s of thi s change?

    4) D o long-term adapti ve ef f ects occur w i thhigh-f i ber diets?

    5) W hat interacti ons occur betw een f iberand other m ineral s and dietary consti tuents?

    6) Is the change in m ineral balance signi f i -cant in biological terms?

    I t i s possible that f i ber i tsel f , i ndependentof phy tate, i nterf eres w i th m ineral absorpti onand metabol i sm . Rev iew of the botanical l i t-erature quick l y heads one to the bel i ef thatnot only do cel l w al l substances themselvesbind calcium and other cations but al so thatthese cations play an essential role in thedevelopm ent of the plant cel l w al l and inplant grow th. D etai l ed calcium -binding stud-ies hav e been reported w i th poly sacchar idesf rom cel l w al l s 54) , and in v i tro w ork sug-gests that f i ber may indeed bind calcium (55),possibl y in relati on to the uronic acid com -ponent of the cel l w al l structures (56). Ca -cium binding di rectl y to f i ber may be part ofthe explanation f or negati v e m ineral balancesin subjects fed high-f i ber diets (48). A t thepresent time l i ttl e is know n about the ef f ectof f eeding f iber f rom sources other than cer-eals on m ineral balance in man; w ork in thi sarea is clearl y needed.

    Equal l y important i s the suggestion thatthese changes in calcium balance are in factonly short term and that over a course ofw eeks and m onths man is able to adapt to theal terati ons in intesti nal physiology and returnto normal calcium balance. W alk er et a . (57)w ere among the f i rst to suggest that, i f sub-jects w ere studied f or long per iods (over 4w eeks), cal cium balance w ould return to nor-mal . A num ber of f actors in W alker s studymakes interpretati on di f f i cul t, parti cularl y

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    S26 CU M M IN G S

    the large f al l i n calcium intak e w hen subjectsw ere transferred f rom thei r normal diet to thestudy diets ( i .e., a change in calcium intakef rom 1000 to 500 m g/day). I nteresti ngl y , thesubject w ho norm al l y took the low est calciumintak e show ed no change in calcium balancew i th w hole m eal bread. Campbel l et a . (58)w ere unable to show adaptati on in calciumbalance to w hole w heat diets in tw o subjectsw hom they studied over a per iod of 5 to 6w eeks. T hei r tw o subjects remained in nega-ti ve calcium balance throughout the ex peri -m ent, and both show ed a f al l i n serum cal -cium levels.

    Serum calcium lev els have not f al l en inother studies in w hich the ef f ect of supple-m enting a W estern-type diet w i th bran orw hole w heat products has been observ ed ov erper iods of 3 to 19 w eeks (59-6 ) . A signi f i cantexception to thi s pattern, how ever, w as seenin a study of 27 elder l y patients w hose dietsw ere supplemented w i th 10 or 20 g of branfor 6 w eek s (62). T hese f indings clearl y needfurther study .

    Studies in w hich magnesium absorpti onhave been measured at the same time ascalcium absorpti on tend to show the tw ocations behav ing sim i larl y w hen w hole w heatdiets are fed.Zinc

    T he possibi l i ty that m an might becom ezinc def i cient has been taken ser iously onlyin recent years; that f i ber m ay play a part i nthe developm ent of thi s def i ciency i s a newconcept. I ni ti al impetus to thi s w ork cameoriginal l y f rom Prasad et al . (63-66) w hodescr ibed a zinc-def i ciency syndrom e in I ra-nian chi l dren characteri zed by i ron def i ciencyanaem ia, hepatosphenomegaly , hypogonad-i sm , dw arf i sm , and geophagia. T his w as latershow n to be associated w i th impai red zincabsorpti on, and i t i s now clear that grow thcan be improv ed in young people by addingzinc to thei r diet (67). Equal l y startl i ng hasbeen the demonstrati on by H am bidge andW al rav ens (68) that zinc def i ciency occursev en am ong the chi l dren of m iddle- and up-per-i ncome f am i l i es in the U ni ted States. T herole of diet i n promoting or impai ri ng zincabsorpti on therefore becomes crucial .

    Rhinehold et al . (47, 48) show ed that dietshigh in w hole w heat products lead to negati vezinc balance and ini ti al l y suggested that thi s

    w as due to the phy ti c acid content of thesef oods analogous to the calcium mahabsorp-ti on-phy ti c acid story . M ore recentl y he hasshow n that zinc binds qui te strongly , perhapsmore strongly than calcium , to dephy tini zedf iber in v i tro 5 5 69). I n fact the removal ofphy tate f rom bran or w hole m eal bread orthe addi ti on of calcium to the preparati onseem s to increase zinc binding in v i tro. Z inchas also been show n to bind in v i tro to starchand pure cel l ulose.

    I n contrast to thei r f i ndings for calciumabsorpti on, Campbel l et al . (58) suggest thatadaptati on to impai red zinc absorpti on doesin fact occur af ter a period of w eeks. H ow -ev er, f ew long-term studies have been done.Prel im inary ev idence on the properti es ofother f i ber preparati ons has y ielded conf l i ct-i ng resul ts (70, 71).

    Further interest in thi s aspect of m ineralabsorpti on has been stim ulated by the sug-gestion that the rati o of zinc to copper ab-sorbed could be important in the dev elop-ment of atherosclerosi s through an ef f ect oncholesterol m etabol i sm (72). M any questionsrelati ng to zinc absorpti on and f iber remainunanswered.I r o n

    I ron absorpti on i s know n to vary consid-erably depending on the type and composi -ti on of the diet being eaten. I ts av ai l abi l i tyf rom w hole w heat products i s parti cularl ypoor (73). B alance studies show that i ronabsorpti on i s impai red f rom diets containingw holemea bread (74) and f rom test mealscontaining r i ce and vegetables (75). Otherinvestigators have show n decreased serumi ron levels af ter 3 or 5 w eek s of diets contain-ing bran and w hole w heat products (62, 76).O nce again phy ti c acid has been incrim inatedas the main factor dim ini shing i ron absorp-ti on in these ci rcumstances and in parti cularthe f orm in w hich the i ron is bound to phy-tate. I n the rat the monof err i c phy tate presentin bran w as readi l y avai l able f or absorpti onw hen isolated f rom the bran w hi le other bran-i ron-phy tate com phex es w ere not (77). I t i sal so possible that i ron binds di rectl y to plantcel l w al l material other than phy ti c acid (55),so w e need to study i ron absorpti on speci f i -cal l y f rom the point of v iew of dietary f i ber.

    T he interacti on in the gut of cel l w al l ma-ter ial s w i th m ineral absorption represents a

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    possible disadvantage of high-f i ber diets andperhaps parti cularl y so w hen W estern-sty lediets are supplem ented w i th high-f i ber prep-arati ons. One area w here caution w ould seemto be needed is in supplementing the diet ofold people w i th w hole w heat products toimprove bow el habi ts w hen thei r dietary in-takes of i ron and calcium m ay be barelysuf f i cient f or thei r normal requi rements. I t i sdi f f i cul t to di sentangle the relati ve roles ofphy ti c acid and dietary f i ber in al ter i ng m in-eral absorpti on, but current ev idence suggeststhat f i ber m ay hav e an independent role.Further inf ormation i s needed parti cular l y onthe m ineral -binding properti es of dietary f i -ber as present in commonly eaten f rui ts andvegetables. Equal l y im portant to bear in m indw i l l be the possibi l i ty that i n the long termthe hum an system is able in som e w ay toadapt to the dim ini shed avai l abi l i ty of m in-eral s as a resul t of these dietary changes andthat w e may ul tim atel y hav e seemed ov ercau-ti ous about thi s aspect of dietary f i ber m etab-olism.Con c lu s i o n s

    Suf f i cient prel im inary ev idence is avai l ableto suggest that f i ber has important nutr i ti onalim pl i cati ons in addi ti on to i ts al ready w el l -k now n gastroenterological ef fects. Fiber ap-pears to af f ect the rate and route of absorp-ti on and metabol i sm of dietary fat, carbohy-drate, and protein as w el l as al teri ng sterolmetabol i sm and m ineral balance.

    T he important question of the signi f i canceof these changes remains to be answ ered. W eneed f urther inf orm ation bef ore the role ofdietary f i ber can be assessed. For example w eneed to know more about the amount of f i bereaten by various populati ons, i ts type, and i tsphy siological ef fects. G athering thi s infor-mation i s unl i kel y to prov e easy as the essenceof the f iber story i s one of long-term changesin diet l eading to al tered patterns in humandisease. Furtherm ore w e need to recognizethat the nutr i ti onal signi f i cance of a f i ber-r i chor f i ber-depleted diet w i l l depend on otherconsti tuents of the diet, w hich v ary greatl y indi f f erent parts of the w orld. Fiber cannot beseen in i solati on f rom the rest of the diet.

    I t i s w isest to assume at the m oment thatthe absorpti on and metabol i sm of m any i fnot al l nutr i ents are af f ected by f iber. Some

    of these changes appear to be nutr i ti onal l ybenef i cial al though the role of f i ber in mm -eral absorpti on giv es grounds f or concern. I fthe ef f ect of f i ber on colonic f unction prov esto be important in rel i ev ing constipati on andprev enting diverti cuhar di sease and largebow el cancer, the need to increase f iber in-takes w i l l be clear. T his alone means that thenutr i ti onal impl i cati ons need to be evaluated.H ow ever, i t i s now possible to conceiv e thatsom e of these nutr i ti onal changes may be ofequal im portance in thei r ow n right.

    T he author is indebted to D r. Phi l ip James for hel pfuldiscussions during the preparat ion of thi s paper and toW i l l B ranch, H elen H ouston, D r . D av id Jenk i ns, andD r. H ugh W iggins for col l aborat ion in studi es on dietaryf iber .R e f e r e n c e s

    1. W I N I T z M ., D . A . SE E D M A N A ND J. G RA F F . S t u d ie sin m et a b olic n u t r it ion em p lo yin g ch em ica lly d efin eddie ts . I. E xt en d ed feed in g of n or m a l h u m a n a d u ltm a le s . A m . J. Chi n. N utr. 23: 525, 1970.

    2. C U M M I N G S J. H ., M . J. H I L L D . J. A . J E N K I N S J. R.P E AR SO N AN D H . S. W IG G INS . C h a n g es in feca lcom posi tion and colonic funct ion due to cereal f iber.A m. J. C l in. N utr. 29: 1468, 1976.

    3. J O V E R A ., AN D R. S. G O R DO N . P r oced u r e for q u a n -ti tati v e analysis of f eces w i th special reference tofecal f atty acids. J. L ab. Cl in. M ed. 59: 878, 1962.

    4. M C C A N C E R. A ., AN D E. M . G L A S E R . T he energyv alue of oatmeal and the digest ibi l i ty and absorptionof i ts proteins, f ats and calcium . B ri t. J. N utr . 2: 221,1948.

    5. M C C A N C E R. A ., AN D C. M . W A L S H A M . T he di ges-tib i l i ty and absorption of the calori es, protein, pu-rines, f at and calcium in w holemeal w heaten bread.B ri t. J. N utr. 2: 26, 1948.

    6. W A L K E R A . R. P. E f f ect of hi gh crude f ibre i ntakeon transi t ti me and the absorption of nutri ents inSouth A f ri can N egro school chi ldren. A m . J. C l in.N utr. 28: 1161, 1975.

    7. K A Y R. M ., AN D S. T R U S W E L L . Ef f ect of ci truspectin on blood l i pids and fecal steroid secretion inm an. A m . J. Cl i n. N utr. 30: 171, 1977.

    8. J E N K I N S D . J. A ., A . R. L E E D S M . A . G A S S U L L H.H O U S T O N D . V . 00F F A ND M . J. H I L L . T he chol es-terol low er ing properties of guar and pectin. C l in.Sci . M ole. M ed. 51: 8, 1976.

    9. G 0E RING H . K ., C . H . G OR DO N R . W . H EM KE N D .R. W A L D O P. J. VA N S0E ST AN D L . W . SM IT H .A naly ti cal esti mates of ni trogen digestibi l i ty in heatdamaged forages. J. D ai ry Sci . 55: 1275, 1972.10. V AN SO E ST P. J., A ND R. W . M C Q UE E N . T h e ch em -i stry and estim at ion of f i bre. Proc. N utr. Soc. 32:123, 1973.

    11. V AN SO E S T P. J. Food and f i bre. N { 228} ringsf orsk ni ng20: (Suppl . 14) 61, 1976.

    12. S C H N E E M A N B . 0. T he ef f ect of plant f ibre ont r y p sin a n d ch ym ot r yp s in a ct iv it y in vit r o . F ed er a -t ion P r oc . 36: 1118, 1977.

    13. D R A S A R B . S., D . J. A . J E NK IN S AN D J. H . CU M -

  • 7/27/2019 Am J Clin Nutr 1978 Cummings S21 9

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    S28 C U M M I N G S

    M I N G S . T he inf luence of a diet ri ch in w heat f ibre onthe human faecal f lora. J. M ed. M icrobiol . 9: 423,1976.

    14. B A I R D I . M ., R. L . W A L T E R S P. S. DAVIES M . J.H I L L B . S. D R A SAR AN D D . A . T . S O U T H G A T E . Th ee ffe ct s o f tw o d ie ta r y fib r e su p p lem en t s on ga s t r o in -t e st in a l t r a n s it st oo l w eigh t a n d fr eq u en cy a n d b a c -t er ia l flor a an d fa eca l bi le acids in norm al subjects.M etabol i sm 26: 117, 1977.

    IS. F UCHS, H M S . DO R F M A N A ND M . H. F L O C H . T h eef f ect of dietary f iber supplementations in m an. I I .A l terat ion in f ecal physiol ogy and bacterial f l ora.A m . J. Cl i n. N utr. 29: 1443, 1976.

    16. D R A S A R B . S., A ND D . J. A . JENKINS. B acter ia, dietand large bow el cancer. A m . J. C l in. N utr. 29: 1410,1976.

    17. T R O W E L L H. Di e t a r y f i br e i s c h a e mi c h e a r t d i s e a s eand diabetes mel l i tus. Proc. N utr. Soc. 32: 151, 1973.

    18. W A L K E R A . R . P., B . F. W AL K E R A ND B . D . R I C H -ARDSO N. Glucose and fat tolerances i n B antu chi l -dren. L ancet 2: 51, 1970.

    19. J E N K I N S D . J. A ., A . R. L . L E E D S M . A . G A S S U L LB. C O C H E T AN D K . 0. M . M . A L B E R T I . D ecr ea se inpostprandial insul in and gl ucose concentrations byguar and pectin. A nn. I nternal M ed. 86: 20, 1977.

    20. JEFFREYS, D . B . T he ef f ect of dietary f ibre on theresponse to oral l y adm inistered gl ucose. Proc. N utr.S o c . 3 3 : 1 I A 1 9 7 4 .

    2 1 . JENKINS, D. J . A. A. R. L E E D S M A. G A S S U L L T.M S . W O L E V E R D. V. 00F F K. 0 . M M A L B E R T IA ND T. D. R. H O C K AD AY . Un a b so r b a b le ca r b oh y -drates and diabetes: decreased post-prandi al hy per -glycaem ia. L ancet 2: 172, 1976.

    22. K I E H M . T . 0., J. W . AN DE R SO N AN D K . W A R D .B enef ici al ef f ects of a high carbohydrate, hi gh f i berdiet on hypergl ycemi c diabet i c men. A m . J. C l in.N utr . 29: 895, 1976.

    23. DO UG L ASS, J. M . Raw diet and insul in requi rem ents.A nn. I nternal M ed. 82: 62, 1975.

    24. L E E D S A . R ., M . A . G A S S U L L 0. L . M E T Z A ND D.J. A . JENKINS. Food: inf luence of f orm on absorp-t ion. L ancet 1: 1213, 1975.

    25. JENKINS, D. J . A. A. R. L E E D S . H . H O U S T O N L .H I N K S , K . 0. M . M . A L B E R T I A ND J. H . C U M M I N G S .C arbohydrate tolerance on m an af ter six w eek s ofpecti n adm inistration. Proc. N utr. Soc. 36: 624, 1977.

    26. V A N D ER W EST H U I Z EN , J., M . M B IZ R I AN D J. J.JONES. U nref ined carbohy drate and gl ucose toler-ance. L ancet 2: 719, 1972.

    27. D R O D R I B B A . J. M ., AN D D . M . H U M P H R E YS . D iv-ert i cul ar disease: three studies. Par t I I I . M etabol i cef f ects of bran i n patients w i th di ver ti cular disease.B ri t. M ed. J. 1: 428, 1976.

    28. S O U T H G A T E D . A . T ., W . J. B R A N C H M . J. H I L L B .S. D R A S A R R. L . W A L T E R S P. S. D AV IE S A ND L M .B A I R D . M etabol i c responses to dietary supplementsof bran. M etabol i sm 25: 1129, 1976.29. SO UT HG AT E, D . A . T ., A ND I. D U R N I N . Cal ori e con-version factors. A n ex per imental reassessment of thef actors used in the calculat ion of the energy value ofhum an diets. B ri t . J. N utr. 24: 517, 1970.

    30. W I L L I A M S , R. D ., A ND W . H . O L M S T E D . T he ef f ectof cel l ulose, hem icel lu lose and l ignin on the w ei ghtof stool . A contri but ion to the study of lax ation inm an. J. N utr . 11: 433, 1936.

    31. M I L T O N - T H O M P S O N 0. J., AN D B . L E W I S . Th ebreakdow n ofdi etary cel lul ose in m an. G ut. 12: 853,1971.

    32. W E R C H S. C ., R . W . J U N G H . P L E N K A . A . DA YAN D A . C. I VY . P ect in a n d ga la ct u r on ic a cid a n d theintesti nal pathogens. A m . J. D iseases Chi ldren 63:839, 1942.

    33. S O U T H G A T E D . A . T . F ibre and the other unavai la-ble carbohydrates and thei r ef f ects on the energyvalue of the diet. Proc. N utr. Soc. 32: 131, 1973.

    34. D A W S O N A . M ., C. D . H O L D SW O R T H AN D J. W E B B .A bsorption of short chain f atty acids in man. Proc.Soc. Exptl . B iol . M ed. 117: 97, 1964.

    35. M C N E I L L N . I ., J. H . C UM M IN G S AN D W . P. T .J A M E S . S h or t ch a in fa t t y a cid a b sor p t ion in t h e h u -man large bow l . Gut 18: A 425, 1977.

    36. V AN SO ES T P. J. T he uni f orm i ty and nutri ti ve av ai l -abi l i ty of cel l ulose. Federation Proc. 32: 1804, 1973.

    37. K E Y S J. E., P. J. VA N SO E ST AN D E. P. Y O U N G .Ef fect of increasi ng dietary cel l w al l content on thedigest ibi l i ty of hem icel lu lose, and cel l ulose in sw ineand rats. J. A ni mal Sci . 31: 1172, 1970.

    38. K E Y S J. E., P. J. VA N SoE sr AN D E. P. Y O U N G .Comparati ve study of the digestib i l i ty of f orage,cel lulose and hem icel lul ose in rum inant and nonrum inants. J. A ni mal Sci . 29: I l , 1969.

    39. L U T H E R L ., R. S ANT IN I C. B R E W S T E R E. P E R E Z -S AN T IAG O AN D C . E. B U T T E R W O R T H . F ola t e b in d in gby insol ubl e components of A m eri can and Puer toR ican diets. A la. J. M ed. Sci . 3: 389, 1965.

    40. R U S S E L L R. M ., F. I SM AIL -B E IG I AN D J. 0. R H E I N -H O L D . F o la t e co n ten t s of I r a n ia n b r ea d s a n d t h eeffec t o f t h e ir fib e r con t en t on t h e in t es t in a l a b sor p -t ion of fo lic a c id . Am . J. Chin. N utr. 29: 799, 1976.

    41. N A G A S E H ., AN D A . F U G I T A . T he synthesis of v i ta-m ins by intest inal bacteria in man and the ef f ect ofcel l ulose. I I . Synthesis of thi am ine. J. V i tam inol .Japan 2: 107, 1956.

    42. N A G A S E H ., AN D A . F U G I T A . T he synthesis of v i ta-m ins by intest inal bacteri a in man and the ef f ect ofcel lulose. I . Synthesis of ribof l av i n. J. V i tam i nol .Japan 2: 102, 1956.

    43. C U L L E N R. W ., A ND S. M . O AC E . C ellu lo se a n dpecti n enhance v i tam in B 12 depl etion in rats. Feder-at ion Proc. 36: 1118, 1971.

    44. M A S O N J. B ., N . G IB SoN A ND E. K O D I C E K . Th ech em ica l n a tu r e of t h e b ou n d n icot in ic a c id o f wh ea tbran: studies of nicotin ic acid-contai ning m acromol -ecules. B ri t. J. N utr. 30: 297, 1973.

    45. M C C A N C E R. A ., A ND E. M . W ID D0wS0N . M in er a lm etabol i sm of heal thy adul ts on w hi te and brow nbread dietaries. J. Physi ol . 101: 44, 1942.

    46. M C C A N C E R. A ., AN D E. M . W ID DO W SO N . M in er a lm et a b olism on d ep h y t in ized b r ea d . J. Physi ol . 101:304. 1942.

    47. R H E I N H O L D J. 0., K . N A S R A . L A H I M G A R Z A D E HA ND H . H E DA YA T I . E ffec ts of p u r ified p h y ta te a n dphytate- ri ch bread upon metabol i sm of zinc, cal -ci um , phosphorus and ni trogen i n m an. L ancet 1:283, 1973.

    48. R H E I N H O L D J. 0., B . F A R A D J I P. A B AD I A ND F.I SM A IL -B E IG I . D ec r ea sed a b sor p t ion of ca lc iu mm agnesium , zinc and phosphorus by humans due toincreased f iber and phosphorus consum pti on ofw heat bread. J. N utr. 106: 493, 1976.

  • 7/27/2019 Am J Clin Nutr 1978 Cummings S21 9

    9/9

    N U T R IT ION A L IM PL ICA T IO N S O F D I ET A RY FIB ER S29

    49. B E R L Y N E 0. M ., J. B . A R , E . N ORD AN D R.SH A INK IN . B ed ou in os t eom a la c ia d u e t o ca lciu mdeprivation caused by high phy ti c acid content ofunleav ened bread. A m . J. Cl i n. N utr. 26: 910, 1973.

    50. R H E I N H O L D J. 0. R ick ets i n A si an im mi grants.L ancet2: 1132, 1976.

    51 . F O R D J. A ., E . M . C O L H O U N W . B . M C INT O S H AN DM . 0. D U N N I G A N . B i och em i cal r espo nse of lateri ckets and osteom al acia to a chupatty -f ree diet . B ri t.M ed. J. 3: 446, 1972.

    52 . W I D D O W S O N E. M . Interrelations of dietary cal ciumw i th phy tates, phosphates and fats. N utr. D icta 15:38, 1970.

    53 . R H E I N H O L D , J. 0., H . H E D AY A TI A . L A H IM G A R Z A-D El I A N D K . NA SR . Z in c ca lciu m p h osp h or u s a n dni trogen balances of I ranian v i l l agers fol low ingchange f rom phytate-ri ch to phy tate-poor diets. Ecol .Food N utr. 2: 157, 1973.

    54. D E L U C A S L ., AN D C. E. B U G G . C a lc iu m b in d in g t oD -glucuranate residues: crystal structure of a hy -drated calci um brom ide sal t of D -glucurof l i c acid.Carbohy drate Res. 41: 19, 1975.

    55 . R H E I N H O L D J. 0., F. I5M A IL -B E IG I A ND B . F A R A D J I .Fibre v s. phy tate as determ inant of the av ai l abi l i tyof calci um , zi nc and i ron of breadstuf f s. N utr. Rept.I nternat. 12: 75 , 1975.

    56. B R A N C H . W . J., D . A . T . SO U T H G A T E A ND W . P. T .J A M E S . B inding of calcium by dietary f ibre: i ts rela-tionship to unsubst i tuted uronic acids. Proc. N utr .Soc. 34: l2OA , 1975.

    57 . W A L K E R A . R . P., F. W . Fox AN D J. T . I R V I N G .Studies i n human mineral m etabol i sm . 1. T he ef f ectof bread rich in phy tate phosphorus on the metabo-l i sm of cer tain m ineral sal ts w i th special reference tocalcium. B iochem. J. 42: 452, 1948.

    58 . C A M P B E L L 0. J., J. 0. R H E I N H O L D J. S. C A N N E L LAN D I. N O U R M A N D . T he ef f ects of prolonged con-sumption of w hol em eal bread upon m etabol i sm ofcalcium, magnesium, zinc and phosphorus of tw oy oung A mer ican adul ts. Pahl av i M ed. J. 7: 1, 1976.

    59. H E A T O N K . W ., A . P. M AN NIN G A ND M . H A R T O G .L ack of ef f ect on blood l ip id and calci um concentra-tions of young m en on changi ng f rom w hi te tow hol em eal bread. B ri t. J. N utr. 35 : 55 , 1976.

    60. C O N N E L L A . M ., C . L . SM IT H A ND M . S O M S E L .A bsence of ef f ect of bran on bl ood-l ip ids. L ancet 1:496, 1975.

    61. K A Y R . M ., A ND A . S. T R U S W E L L . T he ef f ect ofw heat f ibre on plasm a l ipi ds and faecal steroi d ex-cretion in man. B r i t. J. N utr. 37: 227, 1977.

    62. P E R S S O N I ., K . R A B Y P. F O NT -B E C H A ND E. J E N S E N .Ef f ect of prolonged bean adm inistrati on on serumlev els of cholesterol , i oni sed calcium and i ron in theel der ly . J. A m . G erontol . Soc. 24: 334, 1976.

    63. P R A S A D A . S., J. A . H A L ST E A D AN D M . N A D I M I .Sy ndrom e of i ron def i ciency anem ia, hepatospleno-megal y , dw arf i sm , hy pogonadism and geophagia.A m . J. M ed. 31: 532, 1961.

    64. P R A S A D A . S., A . M I A L E Z. F A R I D H . H . S ANS TEADA . R . SC H UL E R T A ND W . J. DA RB Y. B ioch em ica lstudies on i ron def ici ency anemi a, dw arf i sm andhy pogonadi sm . A rch. I nternal M ed. i l l : 407, 1963.

    65. P R A S A D A . S., A . M I A L E Z. F A R I D . A . S C H U L E R TAN D H . H . SAN DST E AD . Z in c m et a b o lism in n or m a lsand pat ients w i th the syndrome of i ron def i ci encyanem ia, hypogonadism and dw ar f i sm . J. L ab. C l in.M ed. 61: 537, 1963.

    6 6 P R A S A D A . S., A . R . S C H U L E R T A . M I A L E Z. F A R I DAN D H . H . SAN DS T E AD . Z in c a n d ir on d e ficien cies inmale subjects w i th dw arf i sm but w i thout ancy l osto-m i asi s schistosom iasi s or severe anem ia. A m . J. C l in.Nu t r 1 2 : 4 3 7 1 9 63

    67. R O N A G H Y H . A ., J. 0. R E I N H O L D M . M A H L O U D J IP. G H A V A M I M . R. S. Fox AN D J. A . H A L S T E A D .Z i nc supplementation of mal nourished schoolboy sin I ran: I ncreased grow th and other ef f ects. A m . J.Cl in. N utr . 27: 112, 1974.

    68. H A M B I D G E K . M ., AN D P. A . W A L R A V E N S . Z incdef i ci ency in i nfants and pie-adol escent chi ldren. I n:T race Elements in Human H eal th and D i sease. Z incand Copper, edi ted by A . S. Pr asad and D . O ber l eas.N ew Y ork : A cademi c Press, 1976, v ol . 1, pp. 2 1 -32.

    69. R H E I N H O L D J. 0., B . F A R A D J P. A B A DI A ND F.I S M A I L - B E I G I . B inding of zinc to f i ber and othersol ids of w hol ew heat bread. I n: T race Elements inH um an H eal th and D isease. Z inc and Copper, ed-i ted by A . S. Prasad and D . Oberleas. N ew Y ork :A cademic Press, 1976, v ol . 1, pp. 163-180.

    70. S ANDS TEAD H . H ., L . K L E V A Y J. M U N O Z R. J A C O BS. R E C K D . T U C K E R 0. L O G A N L . E E L K E M A 0.I N G L E T r F. D IN T Z I S A ND W . SH UE Y . Z in c a n d cop -per balances in hum ans fed f i ber . Federat ion Proc.36: 1118, 1977.

    71. B E S H G E T O O R D ., C . K IE S AN D H . M . Fox . Z incuti l i sation by hum an adul ts as af f ected by di etarypectin, cel lu lose and hemicel l uhose. Federati on Proc.36: 1118, 1977.

    72. K L E V A Y L . M . Coronary heart di sease: thezinc/copper hy pothesis. A m . J. Cl i n. N utr. 28: 764,1975.

    73. B J O R N - R A S M U S S E N E. I ron absorption f rom w heatbread. I nf luence of v ari ous am ounts of bran. N utr.M etab. 16: 101, 1974.

    74. W I D D O W S O N E. M ., AN D R. A . M C C A N C E . I ronexchanges of adul ts on w hi te and brow n bread diets.L ancet 1: 588, 1942.

    75 . H A L L B E R G L ., L . G A R B Y R. SUW AN IK A ND E.B J O R N - R A S M U S S E N . I ron absorption f rom South-East A sian diets. A m . J. Cl in. N utr. 27: 826, 1974.

    76. J E N K I N S D . J. A ., M . J. H IL L AN D J. H . C U M M I N G S .Ef fect of w heat f i bre on blood l i pids, f ecal steroidexcreti on and serum i ron. A m . J. Chin. N utr. 28:1408, 1975.

    77. M O R R I S E. R ., AN D R. E L L I S . I sol ati on of m onof err i cphy tate f rom w heat bran and i ts bi ological val ue asan i ron source to the rat. J. N utr. 106: 753, 1976.