malabsorption associated with diarrhea and intestinal infections

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    1248 The Am e ric an Jou rn a l o f C lin ica l N u tr itio n 30 : A UG UST 1977 , pp . 1248-1253. P rin te d in U .S .A .

    M a labso rp tio n assoc ia ted w ith d ia rrheaand in tes tin a l in fec tions13

    Ir w in H . R o senberg ,4 M.D., Noel W . S o lom o ns,5 M .D ., a nd R ob erto E . Schne id er ,6 M .D .

    ABSTRACT A n ep iso de o f d ia rrhe a ca uses w e ig h t lo ss a nd a tem pora ry ce ssa tio n o f g row thin in fan ts and ch ild ren . D ia rrhea is a ccom pan ied b y m a lab so rp t ion o f s ug a rs , n itrog en , fa ts , a ndm ic ro nu trie n ts . Th e m echan ism s b y wh ich acu te d ia rrh ea l d isea se pro du ce m a lab so rp t ion haveno t be en stud ied ca re fu lly . T he n u tr itio na l c os ts o f m a lab so rp t ion m ay po se a m a jo r th rea t ifd ia rrh ea b ecom es ch ro n ic o r recu rren t. Th e hyd ro ge n bre a th te s t fo r c a rboh yd ra te m a la bso rp tiondo es no t re qu ire in tu ba tio n o r b loo d d raw in g an d can be used in ch ild re n to h e lp c la rify theim por tan ce o f ca rbo hyd ra te in to le ra nce in th e du ra tion an d perp e tu a tion o f acu te d ia rrh ea a ndin te s t ina l ba c te ria l ove rg row th . Am . J . C lin . N u tr. 30 : 12 48 -12 53 , 19 77 .

    D ia rrhea m ay w e ll be the comm onest d is -ease/s ym p tom in the wo rld . In C en tra lAm e rica a m a jo rity o f ch ildhood dea ths a reassoc ia ted w ith d ia rrhea (1 ). M o rb id ityfrom d ia rrhea l d isease m ust be m easu redno t on ly in te rm s o fthe life-threatening ef-fe c ts o f w a te r and e lec tro ly te lo ss , dehyd ra -tion , and seps is bu t a ls o in te rm s o f theim pact on g row th and nu tr itio n in ch ild renunde r the age o f 5. It is w el l d oc um en te dtha t an ep isode o f acu te d ia rrhea resu lts in ad rop in w e igh t and a tem po ra ry cessa tion o fg row th in in fan ts and ch ild ren (2 ). S eve ra lfa c to rs a re in vo lved in th is detr im en ta l e f-fe c t on nu tritio na l s ta tu s o f the ch ild . T hesefac to rs in c lude w ithd raw a l o f food , sh ift o ffood from a more nu tr itio us d ie t to one o fs ta rchy g rue ls , the nu tr itio na l cos ts o f in fe c -tion , and the im pact o f d ia rrhea l d isease onthe abso rp tion and u tiliz a tion o f nu tr ien ts .W e w ill e xam ine the ev idence fo r the tem -po rary m a labso rp tion synd rom e w hich oc-cu rs in assoc ia tion w ith d ia rrhea l d iseaseand eva lua te the scope o f th is p rob lembased on pub lis hed repo rts . T he o the r fa c-to rs wh ich in fluence the e ffe c t o f in fe c tiousd ia rrhea on nu tr itio na l s ta tu s a re d iscussede lsewhe re .

    W e w ill firs t e xam ine the scope o f thep rob lem by rev iew ing the ev idence tha t nu -tr ien t m a labso rp tion ex is ts in acu te d ia r-rhea l d isease and the docum en ta tion o f ind i-v idua l nu tr ien t m a labso rp tion . W e w ill e x -p lo re the regu la rity w ith wh ich d ia rrhea l d is -ease o f d iffe ren t e tio log ie s p roduces m a lab -

    so rp tion , and we w ill e xam ine the poss ib lem echan ism s by w h ich in fe c tious d ia rrheam ay p roduce a trans ien t bu t s ign ific an t m a l-absorption synd rom e . F ina lly , w e w ill d is -cuss som e o f the poss ib le nu tr itio na l im p li-ca tions o f m a labso rp tion in d ia rrhea l d is -ease .

    Malabsorp t ion o f n utrien tsTable 1 presents a listing of the nutrients

    the malabsorption of which has been docu-m en ted in m an in assoc ia tion w ith d ia rrhea ld isease or in tes tin a l in fec tio n . T he la rg es tnum be r o f s tud ie s a re re fe rab le to m a lab -so rp tion o f suga rs (3 -15 ) and fa ts (4 , 6 , 16 ).C ons ide r ing tha t suga rs rep resen t the endp roduc t o f d iges tion o f s ta rches , the com -m onest sou rce o f d ie ta ry ca lo r ie s in m os t o f

    F rom th e U n iv e rs ity o f C h ic ag o P ritzke r S ch oo l o fM ed ic ine an d the Ins t itu te o f N u tri tion o f C en tra lAm er ica a nd Panam a .

    2Supported in p a rt b y the W om en s P ro g ram of th eG a stro in tes tin a l R e sea rch Founda t ion .

    2Address rep rin t re qu ests to : I rw in H . R o sen be rg ,M .D ., P ro fe sso r o f M ed ic in e , U n ive rs ity o f C h ica goP ritzk e r S cho o l o f M ed ic ine , 95 0 Ea st 59 th S tree t,C h ica go , Illin o is 60 63 7 .

    P ro fes so r o f M ed ic ine , H ead , S ec tio n o f G as tro en -te ro lo gy , U n ive rs ity o f C h ic ago P r itzk e r S ch oo l o fM ed ic ine , C h icag o , I llin o is 606 37 5Fa cu lty F e l-low o f th e Jos iah M acy Jr. F ou nda tio n ; ho lds a Fu tu reLea de rs A wa rd o f th e Nu trition F ounda tion . U n ive r -s ity o f C h ica go P ritzke r S choo l o f M ed ic ine , C h ica go ,Illino is 60 637 . 6D iv is io n de B iom ed ica , Ins titu teo f N u tritio n o f C en tra l Am erica an d Panam a , G ua ta -m a la C ity , G ua tam a la .

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    MALABSORPT ION , D IARRHEA , A ND INTEST INA L IN FEC T IONS 1249TABLE 1N utrie n t m a lab so rp t ion in acu te d ia rrhe a l d is ease

    Nutr ient Reference

    Suga rM onosa ccha ride s (g luco se , 3-15

    x y lose )D isa cch a r ide s (la c to se ) 6 , 8 , 1 2 -1 5 , 17

    N itro ge n , p ro te in , am in o a c id s 1 8 , 19Fa t 4 , 6 , 16V i taminsB ,2 4, 7 , 2 0 -2 2

    Folate 7 , 2 3V itam in A 24 , 25

    M in e ra ls a nd trace e lem en ts 26 , 27

    the w o rld , the po ten tia l im pact o f d ia rrhea ld is ease on ene rgy use is em phas ized he re .Indeed , p re lim ina ry resu lts from a de ta ileds tudy in G ua tem a la ind ica te tha t m ode ra ted ia rrhea m ay resu lt in an in creased ca lo rielo ss in s too l o f 500 to 600 ca l/day .

    S o lid ev idence ex is ts a lso fo r n itrogen ,am ino ac id , and p ro te in m a labso rp tion (18 ,1 9) . In certain types o f d iarrheal disease,the re is lo ss o f excess ive p ro te in from thegas tro in te s tina l tra c t b y p ro te in - lo s ing en -te ropa thy (3 ). E x tens ive s tud ie s o f v itam inand tra ce e lem en t abso rp tion a re no t ava ila -b le , bu t docum en ta tion o f m a labso rp tion o fv itam in B12 is regu la r in s tud ie s o f patien tsw ith in te s tina l in fe c tion (4 , 7 , 20 -22 ), andthe iso la ted repo rts o f the m a labso rp tion o ffo la te (7 , 23 ) and v itam in A (24 , 25 ) sug -ges t tha t m a labso rp tion o f bo th w a te r- andfa t-so lub le v itam ins occu rs w ith d ia rrhea.E xcess ive lo ss o f m agnes ium has been seenin acu te en te r itis (26 ), bu t de fin ite ly im -pa ired abso rp tion of th is m ine ra l has no tbeen docum en ted . A n im a l m ode ls o f in fe c-tious d ia rrhea have show n m alabso rp tion o ftra ce e lem en ts such as z in c (27 ), bu t suchs tud ie s have no t ye t been pe rfo rm ed in m an .

    W e ca ll spec ia l a tten tion to the p rob lemQ f suga r m a labso rp tion in acu te d ia rrhea ld isease . T he wo rk o f D r. T o rres-P inedo andh is assoc ia te s (10 , 11 ) has e legan tly docu -m en ted the seve rity o f g lu cose m a labso rp -tion in ch ild ren w ith acu te d ia rrhea l d isease .M a labso rp tion has been con firm ed in a w ideva rie ty o f en te r itis , u s ing the nond ie ta rypen tose , x y lo se , as the tes t suga r. M a lab -so rp tion of la c to se is a p rob lem o f spec ia lim po rtance fo r tw o reasons . F irs t, th issuga r, w h ich ist h e ma j o r c a r b o h y d r a t e i nm ilk , is the m ost poo rly abso rbed o f a ll

    d isaccha rides . S econd , in te s tina l la c ta se isthe m ost sens itive of the in te s tina l d isac -cha ridases to in fe c tious , to x ic , o r m e tabo lici n j u r y , a n d t h e r e f o r e l a c t o s e ma l a b s o r p t i o nis one o f the m o re sens itiv e ind ica tors o fm ild in te s tina l in su lt. L ip sh itz and co l-leagues s tud ied 50 M ex ican in fan ts w ith se -ve re d ia rrhea and found 46% w ith la c to sein to le rance , 10% in to le ran t to o the r d is ac-cha r idases , and 6% w ho cou ld no t to le ra tem onosaccha rides (13 -15 ). S uga r m a lab -so rp tion , they suggest, m ay no t on ly w o rsend ia rrhea l s ym p tom s bu t m ay a lso con tr ibu tesubs tan tia lly to the pe rpe tua tion andw o rsen ing o f bac te r ia l o ve rg row th . Thep rob lem o f repea ted b lood tes ts to docu -m en t lac to se m a labso rp tion in sm a ll c h il-d ren w ith d ia rrhea l d is ease has p rec ludedex tens ive s tudy o f the p rob lem o f trans ien tla c to se m a labso rp tion , bu t w ith the m o renew ly deve loped non invas ive b rea th te s tsbased upon e leva tions in b rea th hyd rogen insuga r m a labso rp tion (28 ), it is like ly tha t theseve r ity and du ra tion o f the p rob lem o f la c-to se in to le rance w ith acu te d ia rrhea l d iseasew ill be m o re fu lly e lu c ida ted .Categories of infection associated w i thmalabsorption

    Tab le 2 p resents the p rob lem o f m a lab -so rp tion in d ia rrhea l d isease from the s tand -TABLE 2Po s it ive a ssoc ia tio n o f m a labso rp tio n an d in fe c tion inma n

    I nfecti on Ref erenceB ac te r ia l e n te ritis

    S a l mo n e l l a 20Sh ige l laVibrio cho lerae 7

    V ira l en te ritisNorw a lk agen t 5, 6

    Nonsp ecific gas troen te ritis 4 , 7 , 29P ro to zo a l en te ritis

    G iar d ia lam blia 3 2Cocc id ios is 16 , 3 0 , 31

    P ara sitic In fes ta t ionHookworm 35 , 3 6F ish ta pewo rm 21 , 2 2Ascar ias is 2 4 , 2 5 , 3 4Strongy loidias is 37

    S ystem ic d iso rde rsM ea s le s 3Tuber cu los is 8 , 1 8S ys tem ic b ac te r ia l se ps is 25S tre p toco cca l in fec tio ns 17

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    1250 ROSENBERG ET A L .po in t o f d iffe ren t e tio log ie s . T h is tab le em -phas izes the obse rva tion tha t w heneve r in -te s tina l in fe c tion is su ffic ien tly seve re top roduce d ia rrhea , m a labso rp tion a lso re -suits. Thus , d ia rrhea l d isease and in te s tina lin fe c tion assoc ia ted w ith bac te ria l en te r itis(7 , 20 ), v ira l en te r itis (3 ,, 6 ), n on sp ec ificgas troen te ritis (4 , 7 , 29 ), and p ro tozoa l (16 ,30 -32 ) and pa ras itic in fe c tions (2122 , 24 ,25, 33 -35) have a ll been docum en ted to beassoc ia ted w ith m a labso rp tion . Indeed, ce r-tam sys tem ic d iso rde rs no t d ire c tly in vo lv ingthe in te s tine have been show n to p roducesom e e lem en t o f m a labso rp tion pa rticu la r ly ,if no t exc lu s ive ly , w hen sys tem ic in fe c tionresu lts in a trans ien t d ia rrhea l s ynd rom e (8 ,17 , 18 , 23 , 25 ).

    S om e o f the s tud ie s o f xy lo se and fo licac id abso rp tion b y L i n d e nb a u m (7 ) in pa -tien ts w ith cho le ra and re la ted d ia rrhea l d is -ease a re in s tru c tive fo r the ir docum en ta tiono f the fin ite pe riod o f m a labso rp tion w h ichm ay be assoc ia ted w ith acu te bac te ria l d ia r-rheas . S im ila rly , the trans ien t natu re o facu te v ira l in fe c tion -induced m a labso rp tionhas been w e ll re v iew ed by B lack low and h isassoc ia te s in the case o f e x p e r i me n t a l v i r a li n f e c t i o n wi t h t h e No r wa l k a g e n t ( 6 ) . I nthese s tud ie s , trans ien t m a labso rp tion w asobse rved even in in fe c ted pa tien ts whofa iled to ma n i f e s t c l i n i c a l d i a r r h e a .

    The ev idence fo r m a labso rp tion in p ro to -zoa l and o the r pa ras itic in fe c tion is con flic t-ing . T rans ien t m a labso rp tion due to G ia rd iain fe c tion w ith in vas ion o f the in te s tina l m u -cosa is c lea r ly docum en ted (32 ). O n theo the r hand , m ilde r fo rm s o f acu te g ia rd ia s ishave been s tud ied and m a labso rp tion hasno t been found (33 ). S im ila r ly , the re a rerepo rts o f som e deg ree o f m a labso rp tionw ith A sca ris (24 , 25 , 34 ), hookw o rm (35 ,36 ), and o the r pa ras itic in fe c tions o f thegas tro in te s tina l tra c t (2 ). In a recen t s tudyin ru ra l G ua tem a la , m ild to m ode ra te in te s-tina l pa ras itic in fe s ta tion w as no t re la ted toab ility to abso rb ca lo rie s , n itrogen , and fa tfrom a m ixed d ie t (R . S chne ide r, pe rsona lcommun ica t ion ) .

    T he ba lance o f ev idence seem s to ind ica tetha t m a labso rp tion w ith in te s tina l pa ras ite sis irregu la r and m ild and tha t the nu tritio na lim po rtance o f such m alabso rp tion is unce r-ta in (33 , 38 -41 ), e x cep t in the case o f the

    b lood lo ss and iron defic it seen in hook-w o rm and sch is to som a l in fe s ta tion .Pathogenesi s of m alabsor p t i on in pat i en t sw ith diarrheal disease

    The m echan ism by wh ich acu te d ia rrhea ld isease p roduces m a labso rp tion has no tbeen s tud ied ca re fu lly . H ow eve r, the le s -sons lea rned from s tud ie s o f ch ron ic in te s-tina l bac te r ia l o ve rg row th , p ro te in -ca lo r iem a lnu tr itio n , and o the r fo rm s o f m o re pe r-s is ten t in te s tina l m ucosa l dam age m ay we llbe app lied to an eva lua tion o f the m echa -n ism s of m a labso rp tion in acu te d ia rrhea ld is ease . T he fram ew o rk o f poss ib le m echa -n ism s is p resen ted in T ab le 3 . M a labso rp -tion cou ld occu r because o f even ts in thelum en o f the in te s tine w h ich in te rfe re w ithno rm a l d iges tive and abso rp tiv e p rocesses .O f these p rocesses the one wh ich is pe rhapsm ost suscep tib le to in te rfe rence is the im -po rtan t p rocess o f m ice lle fo rm a tion , w h ichis dependen t upon a no rm a l b ile ac id m e tab -o lism and wh ich is requ ired for the no rm a labso rp tion o f d ie ta ry fa t (42 ). W e a re no tsu re whe the r trans ien t p rox im a l in te s tina lbac te ria l o ve rg row th occu rs in a ll cases o facu te d ia rrhea l d is ease , bu t it is like ly fromthe s tud ie s in G ua tem a la tha t trans ien t in -te s tina l bac te ria l o ve rg row th is comm on un -de r these c ircum stances (43 ). D econ juga-tion o f b ile sa lts in the p rox im a l in te s tine inthe p resence o f abno rm a l bac te r ia l o ve r-g row th is w e ll docum en ted (44), and th ism echan ism cou ld in te rfe re w ith the in te s-tina l abso rp tion o f fa t.

    O the r de tr im en ta l e ffe c ts o f p rox im a lTABLE 3M ala bso rp tio n in d ia rrh ea l d ise ase : p a tho gene t icfac tors

    Framework of poss ble mechanismsA . In tra lum in a l even ts

    1 . Ba cte ria l ove rg row tha . co mp etitio nb . m e tabo lism ( fe rm en ta tio n )c. gasd . s ho rt ch a in fa tty ac idse . b ile a c id s

    2 . O sm o tic e f fec tsB . C e llu la r even ts

    1 . P ha rm a co to xic

    C . 2 . C yto tox icV illou s ab no rm alit ies

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    M ALABSO RPT ION , D IA RRHEA , AN D IN TES T IN AL INFEC T ION S 1251

    bac te ria l o ve rg row th have been obse rved .Th e bacte r ia l m ass is capab le of com pe tingw ith the hos t fo r the up take o f inges tednu trien ts ; th is phenom enon is w e ll de -sc ribed in the case o f v itam in B12 (45 ). F u r-the rm o re , the effe c ts o f bac te ria l m e tabo -lism of ingested nutrients may be important.Bacte r ia l fe rm enta tion o f suga rs occu rs w ithp roduc tion o f gas and sho rt-cha in fa tty ac id s(46 ), bo th o f wh ich a re capab le o f p roduc -ing gas tro in tes tina l sym p tom s and inc reasedw a te r lo ss . D econ juga ted b ile ac id s them -se lves m ay be irrita ting to the in te s tina l m u -cosa and m ay con tribu te to d ia rrhea by the irown cathartic effects (47). Furthermore,fa ilu re to d iges t and abso rb suga rs such asla c tose o r sucrose o r the o ligosaccha ridep roduc ts o f s ta rch d iges tion m ay resu lt in anin creased osm o tic load in the gas tro in te s -tina l lum en and the reby con tr ibu te to d ia r-rhea w ith seconda ry e ffe c ts on v itam in andm icronu trien t abso rp tion . F ina lly , the co r-re la tion be tween ca rbohyd ra te m a labso rp -tion and bacte ria l coun ts in the in te s tine ,repo rted p rev ious ly (13 ), s ugges ts tha t ca r-bohyd ra te m a labso rp tion m ay con tr ibu te to ,a s we ll a s resu lt from , bac te r ia l con tam ina -tion o f the gut.

    The second m a jo r ca tego ry o f pa thogen -es is re la te s to the in te s tina l ep ithe lium andits re sponse to tox in s from the lum en o f thein te s tine . S uch tox in s can be ca tego rized intw o gene ra l g roups : the pha rm aco tox icagen ts , w h ich p roduce an abno rm a lity o fin te s tina l ep ithe lia l func tion w ithout p ro -duc ing a m o rpho log ica l change , and the cy -to to x ic agen ts , w h ich cause dam age w ith o rw ithout in vas ion o f the in te s tina l ep ithe -hum . An exam p le o f the fo rm e r is cho le ratox in (48 ) and an exam p le o f the la tte r isS h ige lla to x in (49 ). C u rren t ev idence ind i-ca tes tha t the pha rm aco tox in s such as cho l-era en te ro tox in do no t a ffe c t in te s tina l ab -so rp tion o f suga rs and am ino ac id s . Indeed ,the fac t tha t suga r abso rp tion is in ta c t incho lera is used as the bas is fo r o ra l the rapyw ith so lu tions con ta in ing g lu cose . H ow eve r,the e ffe c t o f such tox in s on ne t flu id excre -tion m ay ve ry w e ll in fluence the abso rp tionand d ispos ition o f w a te r-so lub le nu trien tssuch as fo lic ac id . S h ige lla to x in con tr ibu testo a cy to to x ic e ffe c t w h ich in te rrup ts no rm a lin te s tina l ep itheh ia l p rocesses , re su lting in

    de fec ts in in te s tina l abso rp tion . Cyto tox ice ffe c ts o f in te s tina l in fe c tion m igh t be p ro -duced no t on ly by bac te r ia l to x in s bu t a lsoby m e tabo lite s o f endogenous o r exogenousmater ia ls .

    A cu te in te s tina l in fe c tion from a va rie tyo f causes m ay be assoc ia ted w ith m o rpho -log ica l and even v illo us abno rm a litie s o f thein te s tina l m ucosa s im ila r to those assoc ia tedw ith m o re seve re ch ron ic fo rm s o f m a lab -so rp tion . The re is o ften a m a rked los s o fabso rb ing su rfa ce . S uch m o rpho log ica l ab -no rm alities m ay re fle c t the tox in e labo ra -tion o f the o ffend ing o rgan ism , and the rem ay be d irec t in vas ion of the m ucosa .

    Im pa c t o f in fec t io n -a ssoc ia t edm a la b sor p t io n on n u t r it ion a l st a tu s

    A g rea t dea l o f w o rk is le ft to be done onassessm en t o f the nu tritio na l im pact o f them a labso rp tion wh ich is assoc ia ted w ithacu te d ia rrhea l d isease . O bv ious ly , the se -ve r ity o f the nu tr itio na l de fic it is re la ted tothe du ra tion and m agn itude o f the m a lab -so rp tion in each ind iv idua l s itua tion . In fa c t,the cos ts o f m a labso rp tion in d ia rrhea l d is -ease ra re ly pose a m a jo r th rea t to nu tri-tio na l s ta tu s un le ss d ia rrhea becom esch ron ic o r re cu rren t. T hen , the downw a rdsp ira l o f food w ithd raw a l, m a lnu tritio n ,d ia rrhea , m a labso rp tion , e tc ., th rea tenslife . A ce rta in pe rcen tage o f ch ild ren w ithacu te d ia rrheah d isease o f nonspec ific causehave pe rs is ten t ca rbohyd ra te in to le ranceand the re fo re unde rgo a m uch m o re seve reand p ro longed nu tritio na l de fic it. C oe llo -Ramirez and L ipsh itz repo rted tha t 18% o f403 M ex ican ch ild ren w ith d ia rrhea hadpe rs is ten t d ia rrhea and ca rbohyd ra te in to l-e rance (13 ). L indenbaum found tha t 18 o f52 pa tien ts w ith d ia rrhea in B ang ladeshfa iled to recove r no rm a l abso rp tion w ith in 2weeks (7 ). N ew non invas ive techn iques o fassess ing bac te r ia l o ve rg row th and ca rbohy-dra te in to le rance p rom ise to add g rea tly toou r ab ility to s tudy the cos ts and causes o fch ron ic d ia rrhea . The recen tly descr ibed hy-d rogen b rea th te s t fo r ca rbohydra te m a lab -so rp tion w h ich is perfo rm ed in ch ild renw ithou t in tuba tion o r b lood d raw ing (36 )shou ld c la rify the im po rtance o f ca rbohy -d ra te in to le rance in the du ra tion and pe r-

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    1252 ROSENBERG ET A L .pe tua tion o f acu te d ia rrhea and bac te ria lo ve rg row th . C oup led w ith the b ile sa ltb rea th te s t o f bac te r ia l o ve rg row th (50 ),w h ich can now be pe rfo rm ed w ith non rad io -ac tive 3C ra the r than 4C (51 ), thus obv ia t-ing any haza rd in in fan ts and ch ild ren , suchtes ts w ill pe rm it a ssessm en t o f the re la tiveim po rtance o f ca rbohyd ra te fe rm en ta tion ,bac te ria l ove rg row th , and b ile sa lt m e tabo -lism in the ch ron ic ity o f ch ildhood d ia rrhea .The hyd rogen b rea th te s t a lso p rom ises tobe use fu l in assess ing ou r ab ility to in te rvenewi t h h i gh - c a l or i e n u t r i t i on a l d i e t s e a r l y i nthe cou rse o f ch ildhood d ia rrhea be fo re fu r-the r nu tr itio na l de fic it is added to tha t w h ichso o ften unde rlie s the d ia rrhea l ep isode .U

    Re fe re n c e s1. SCR IMSHAW, N . S ., C . E . TAYLOR AND J . E . GOR -

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