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C om m unity and International N utrition

Stunting is Associated with Overweight in ChildreFour Nations That Are undergoing the NutritionTransition1 i

BARRY M. POPKIH 2 MARIE K. RICHARDS AND CARLOS A. MOHTIERO

D epartm ent of Nutrition, School of Public H ealth, and C arolina Population Center, U nNorth Carolina at Chapel H ill, Chapel H ill, N C 27516-3997 and Center for Epidem iolStudies in Health and Nutrition, D epartm ent of Nutrition, School of Public H ealth, USÃ o P au lo , S Ã o P au lo , B ra zil

ABSTRACT A higher risk of obesity in stunted child ren has been desc ribed in Hispan ic -Amer ican , Jamai

can and A ndean pop ulations, b ut little system atic exp loration has been done concernin g this area in n utrition. This paper exam ines the relationship betweenstu ntin g an d overw eight statu s for children aged 3-6and 7-9 y in nationally rep resen tative su rveys in R ussia, B ra zil, an d th e R ep ub lic o f S ou th A fr ica a nd a larg enationwide survey in China, using iden tical cut-o ffs fo rbod y m ass ind ex, the prevalen ce of ch ild overw eightin these countries ranges from 10.5 to 25.6% (basedon th e 85th percentile); recen t N HA NES H Iresults indicate that this prevalence is around 22% in the U.S.S tu ntin g is also com mon in the su rveyed coun tries affectin g 9.2-30.6% of all children . O ur resu lts show eda significan t association b etw een stu nting and overw eigh t sta tu s in ch ild ren of a ll co un tries. T he in co me -

adju sted risk ratios of b ein g overw eight for a stun tedchild ranged from 1.7 to 7.8. Clearly, there is an impor tant associa tion between s tunting and h igh weight-fo r-h eigh t in a v ariety o f eth nic en viro nm en ta l a nd social backgrounds. A lthough the underlying m echan ism s rem ain u nex plore d, th is a sso cia tio n h as serio uspublic health implicat ions par ticular ly for lower incomecountr ie s. As these countr ie s ente r the nutr ition transitio n ex per ien cin g la rg e c ha ng es in d ieta ry an d a ctiv ityp attern s, they m ay face, am on g oth er p rob lem s, add itiona l d ifficultie s in their fight aga inst obesity. J . Nutr.126:3009-3016, 1996.

INDEXING KEY WORDS:

â €¢h um a ns â €¢c hild o be sity â €¢ tu ntin g•prog ram ming

There is limited documentation showing that sub-populations of Hispanic-Am erican, Jam aican, and An

dean children are stunted and obese or overw eight Ad-rienzen 1973, Forrester et al. 1996, M artorell et al.1987, Trowbridge et al. 1987 . At the same time, various hypotheses propose that nutritional insults duringpregnancy or infancy may have long-term effects on awide range of metabolic and other physiological relationships Barker 1992 and 1994 . Barker and his colleagues have shown that adults with low weight at age1 y or low birth weights have a greater tendency tostore fat abdominally Law et al. 1992 . In addition,R avelli et al. 1976 found that m ales w ho experiencedfamine during the first half of gestation were m orelikely to becom e obese as young adults. W e presentinform ation on the distribution of the relationship between stunting and overweight status over a range ofenvironm ents and genetic backgrounds. This relationship between stunting and fat deposition was not apparent prior to the shift in incomes and the relatedchanges in diet and activity levels in most low incomecountries, because stunted children had little opportunity, in terms of economic conditions, lifestyles, andresource availability, to becom e obese. The em ergenceof this nutrition transition with its rapid shifts in thecom position of diet and activity patterns and subsequent shifts in body composition suggests that this relationship m ight lead to considerable obesity over thenext several decades, affecting individuals living in environments in which current infant feeding and mor

bidity patterns during infancy are associated with extensive stunting Popkin 1994 . Rapid shifts in the

1 Th e c os ts o f p ub lic atio n of th is a rtic le w ere d efra yed inth e p aym en t o f p age ch arges. T his ar tic le m ust th ere for e b em ar ked a d ver tise men t in a cco rd an ce w ith 1 8 U SC se ctionso le ly to in dica te th is fa ct.

1 To w ho m co rresp on de nce s ho uld b e a dd re ssed .

0022-3166 /96 3 .00 ©1996 Amer ican Ins ti tu te of Nutr it ion.M an usc rip t re ce iv ed 2 6 F eb ru ar y 1 99 6. I nitia l re vie w co mp le ted 7 A pril 1 99 6. R ev isio n a cc ep te d 2 1 A ug ust 1 99 6.

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3010 POPK IN ET A L.

structure o f d ie ts and ac tiv ity patterns might le ad to am ajor problem of obesity am ong these stunted children. This article attempts to direct research attentiontoward this topic .

It is possible that linkages between stunting and obesity are biological in origin. B arker (1992 and 1994)suggests that an infant's major adaptation to undernu-

trition is a reduced growth rate and re lated changes infe tal hormone produc tion that y ie ld long-te rm effectsincluding changes in insulin and grow th horm one.Barker has also found in a series of studies on sm allsamples of English adults that low birth weight (particularly d isproportionate growth) was re lated to subsequent abdominal obesity and a wide range of hormonalchanges , associated with syndrome X (Barker 1992). Inaddition, he has shown that growth retardation is associated w ith later obesity and a range of horm onalchanges. A rap id ly emerg ing lite rature is revealing animportant role related to diabetes and other biologicalcomplications for fe tal and infant nutritional insults

in the U.S . and e lsewhere (Forreste r e t al. 1996, Haleset al. 1992, Valdez et al. 1994), but few hav e linkedthis w ith obesity. O thers, includ ing Dietz (199 4) andKumanyika (1993)link very high birth weight to subsequent obesity. These may represent two separate mechanisms, one associated with the effects of undernutri-tion during pregnancy and infancy, and the o ther wi thgestational diabetes and poor diet. M any others in awide range of f ie lds, including a recent Nobel Laureatein economics (Fogel 1994 ), have related sho rtness, amarker of deprivation early in life , to subsequent morbidity and m ortality problem s, ev en w hen body m assindex (BMI)3or weight is controlled for.

The age at w hich stunting might relate to the develo pment o f o besity is unclear. Child ren have four periods of c ritical weight gain: the third trimeste r of gestation, early infancy, at age 5-7 y (ad ipose rebound) andd uring ad olesc ence (Die tz 1994). S tunting remains amajor problem in most low income countries; its p revalence ranges from 11 in urban African c itie s to 30 -48 i n many A frican, Asian, and Latin Am erican urb an and rural are as (Von Braun et al. 199 3).T he mostcom plete rev iew of this topic estim ates that 43 ofpreschool children in low er incom e countries arestunted (deOnis e t al. 1993).At the same time, changesin incomes and eating p ractice s are clearly lead ing tohigher fat d ie ts among many segme nts o f these so cieties (Popkin 1994).

We examine the re lationship betw e en stunting andoverweight status in child ren in four countries at various stages of econom ic transition. T he m ethods and

3 Abbreviations use d: BMI bo dy ma ss inde x; CHNS China

Health and Nut rit ion Survey ; IBGE, Ins ti tuto Bras il ei ro de Geograf iae Estastistica; LSM S, Liv ing Standards M easurem ents Surv ey,-N CHS, N ational Center for Health Statistics; N HES, N ationalHealth and Examinat ion Survey,- RLMS, Russian Long itud inal Monito ring Survey ; RR, re lat ive ri sk ; TSF, tri ceps skinfold .

databases for information on stunting and ovestatus for the large countries of China, Braz iland the Rep ub lic o f S outh Africa are presentednext section fo llowed by an analysis and a dis

SUBJECTS A ND M ETHO DS

We used data from four large nationw ide sThe collection of the data in China and Russia finformed consent procedures estab lished byUniversity of N orth Caro lina at Chapel Hilltional review board and the institut ional reviewof the C hinese A cadem y of Prev entiv e M edithe R ussian Institute of Sociology, A cadem yences. In both surv eys, familie s we re info rmethe study and its costs and benefits and asked toate. The B raz ilian and South A frican data seco llec ted by o rganizations in those countrie s

lowed procedures established by the Insti tuto Bde Geografia e Estatistica and the Universitytown, respectively. In all cases , a cross-sectionm ation is exam ined. The objectiv e of this stthe analysis of large representative samples ofthat allow ed us to exam ine the relativ e riskw eight am ong stunted children. M oreov er,these data se ts contains measures o f income oditures for the households, w hich prov ide a bcontroll ing for economic status.

Ch in a. T he Ch in a H ealth an d N utrition(CHNS) is an on-going, longitudinal survey thae ight prov inces in China: Guangxi, Guizhou,Hubei, Hunan, Jiangsu, Liaoning and Shangdothough this survey is no t nationally repre sethese p rovinces w e re selecte d to p rov ide sivariab ility in geography, economic deve lopmhealth indicato rs such that they may be consibe general ly representative of al l provinces in ttry. A mult is tage, random, cluster sampling pwas used to d raw the sample fro m each p rovinwere collected from all household members.team s m easured w eight using calibrated, pspring scales with the individuals wearing lighand no shoes. We used data from the CHN S 11993, w ith sam ples consisting of 1755 and 19-y-old children, respectively. Addit ional detresearch design of this survey is presented e l(e .g ., Popkin e t al. 1995).

Russia The Russian Longitudina l Moni toring Surv ey (RLM S) is a househo ld -based survey dem onito r sy stematically the e ffec ts o f the Rufo rms o n the economic we ll-being o f househindividuals. The first nationally representativeof the Russian Federation was deve loped spefor this surv ey. We used data from the first rphase 2 of the 1994/95 RLMS for this survesample of 1106 3- to 9-y-old children. Additio

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RELATION SHIP BETW EEN STU NTING A ND OV ERW EIGHT 3011

on the research design of this surv ey is found elsew here(M roz and Popkin 1995, Popkin et al. 1996). Data collection is identical w ith that for our China survey except that, in C hina, docto rs and nutritionists collectedall data, w hereas in Russia, this w as done by trainednonmedicai inte rv iew special is ts .

Republic of South Africa We used data from the

Living Standards Measurement Survey (LSMS) asadapted by a group of social science researchers inSouth A frica. Collected in 1994, this w as the first attempt to develop a representative sample for the Republic of South A frica. C ensus enum eration districtsw ere used as the first stage w hen possible, and in theform er hom elands, v illages or v illage groups w ere usedw ith a probability proportionate to their siz e. The second s tage was a random sample of nonins titutional izedhouseho ld s, w hich inco rporated mig rant labor ho stels.The final sam ple consisted of 8848 households and inv olv ed 43,974 indiv iduals. The 12.7 of the sam pleaged 0-6 y w as surveyed for w eight and height. For

each child, the exact date of birth w as obtained. Techniques standardized by the World Bank set of LSMSw ere follow ed for collecting w eight and height data.

Brazil Data in this study came from a random national nutrition survey undertaken by the Brazilianagency in charge of national statistics (Instituto B rasi-leiro de Geografia e Estatistica, IBGE), from June toSeptem ber 1989. D etails of the m ethodologies used inthe surv ey hav e been described prev iously (M onteiroet al. 1992). M ultistage stratified clustering sam plingw as used. The surv ey consisted of 14,455 householdsw ith data collected from all household members. Wefocused on children aged 1-9 y (11,109 in 1989).Trained team s m easured w eight using calibrated, portable spring scales w ith the indiv iduals w earing lightclothes and no shoes.

M ea su re s H e ig ht fo r a ge a nd we ig ht fo r h eig ht e xpressed in Z-scores of the National Center for HealthStatistics (N CHSJ/W HO standard w ere used to assessstunting and overw eight for children under age 10 y,respectively (W HO 1986). Child ren w ith height-fo r-agebelow tw o Z -sco res w ere classified as stunted and thosew ith w eight-for-height above tw o Z-scores as overw eight. Weight adjusted for height represents a m easure of ov erw eight and only indirectly m easures obesity (Piegai 1993). D espite the lim itations associatedw ith using w eight-for-height as an indirect m easurement o f child o besity, this ind icato r is the conv entio nalm easure used in m ost population studies of children(G orstein et al. 1994).

BMI represents an alternative measure of overw eight. U nfortunately there is no consistent set of B MIstandards for preschool child ren. L ater, w e present B M Iresults for children aged 6 y and older. W hen these BM Imeasurements of overw eight are used, our results donot change. B ecause this analy sis focuses on childrenaged 3-9 y, w e required a consistent standard for allages and w ere forced to use the w eig ht-for-heig ht index.

W hile there are lim itations and adv antages rto the use of the w eight-for-height index, therea need for a more direct measure of body fat. Idemeasure of total body fat is required that can bfor children in all four countries (cf. B andini and1987, Roche et al. 1981). A s a simplified measbody fat, triceps skinfold has been the site mo

quently selected for a single m easurem ent (B andDietz 1987, D ietz and R obinson 1993). For threecountries in this study, w eight and height w eonly av ailable m easurem ents. In China in 1991fold m easurem ents w ere collected from a subsof children. To determine how our measuremeoverw eight related to a more accurate m easurecess fat, w e examined the mean and median tskinfold (TSF) for C hinese children w ith w eigheights above and below the 85th percentile.w ere 7.5 and 7.0 m m , respectiv ely, for non-ov erwand 8.2 and 7.5 m m, respectiv ely, for ov erw eighdren (i test; P < 0.002). For the same Chinese sa

w e estim ated the risk ratio of ov erw eight for thosa T SF higher than the 8 5th percentile against a m eof w eight-for-height based on ov erw eight at thpercentile. The risk ratio for this relationship ow eight based on TSF w ith that for w eight-for-hw as 3.63 (CI:2.18-6.05). This subset of Chinesedren experienced a low er prev alence of ov erw eiging triceps skinfolds abov e the 85th percentile,on the age-specific cutoffs from N HA NES I andsancho 1990). These results are not unusual, andcern exists that the com parison of triceps skinfoA sian children to a U.S. reference populationrelev ant. For exam ple, A sian adults and adoleshav e more subcutaneous adipose tissue on thethan on their limbs relative to other ethnic g(M alina et al. 1995, Wang et al. 1994). These rsuggest that w e m ust be cautious in interpretingw eight-for-height m easures in the C hinese childind icative o f overwe ight status.

Household income per capita w as used to cfo r access to reso urces. A ll fo ur surveys co llecteddetailed cash and in-kind m easures of incom e, aplete set of expenditures, or both. The incom e pita m easure used in the analy sis for China, RussiBrazil is based on the combination of income fr

sources divided by total household membershiSouth A frica there w as no measure of income.surv ey used an alternate m easure often used bymists, w hich w as total family expenditures foand all other goods and serv ices purchased.

Statistics The risk ratio was used to measure theassociation betw een being stunted and beingw eight, that is, the probability of being ov erw eithe stunted subsample of each population dividthe probability of being ov erw eight in the nonstsam ple. C onfidence interv als at the 0.95 lev el arelated. We present crude and incom e-adjusted riskcalculated according the M antel-Haensz el proc

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3012 POPK IN ET A L.

TABLE 1

Prevalen ce of 6- to 8-y-oI d ch ildren w ith body m ass in dex B M I h igh er th an th e U .S . ref eren ce—N H E S 85thp erc en tile s in f ive co u ntries1

NHES percentilesNHANESIII

(1988-91)SouthRussiaChina (1993) (1994-95) TotalA frica

(1994)Only

blackand coloredBrazil (1

NHES5th3MalesFemalesNHES

85th3MalesFemales11.713.721.324.28.09.214.112.211.88.125.617.87.44.125.020.38.24.523.020.94.63.312.810.5

1 S ource: N ational Health and Exam ination S urv ey (N HES | B MI standards at the 95th and 85th percentiles; personaR ic hard P. Tro iano, N atio nal C enter fo r Health S tatistics, A pril, 1 99 6.

2 S ource of N HA N ES III data: Troiano et al. 1995.3 N ote: 6-8 y is equivalent to 72-108 mo.

(Hennekens and Buring 1987). Income control is essential in this case because income itself can be associatedwith stunting and ove rwe ight (usually in d iffe re nt d irections).

Sa mp le. C hild ren a ged 3 6-119 .9 mo 3 -9 y a r e co nsidered excep t for the South African sample for whichchildren aged 36-91 m o w ere included. The sam plewas separated into 36-83.99 mo (3 -6 y ) and 84-119 .9m o (7-9 y ). Children aged 0-35 m o w ere not considered because it is during this age that m ost stuntingocc urs (Wate rlo w 1988). By 36 mo, m ost stunting hastaken p lace and child ren are p roceeding on a no rm alheight trajectory until adolescence; thus w e can explore the association between stunted status and overweight status.

RESULTS

C hildren in the U nited States are thought to hav ev ery high levels of obesity (Tro iano e t al 199 5).To putchild overweight status in our sample countries in perspectiv e, w e lo oked at the high BMIstatus o f our sample populations in reference to the United States. Comp arisons o f co mbined p revalence estimates fo r overwe ig ht child ren aged 6 -8 y in five national surv eys arepresented in Table 1 to contrast lev els of child ov erw eight status in the U nited States w ith those in oursample countries. The values in Tab le 1 , adjusted fo rage,estimate the percentage of persons in each categoryw ith BM I at or abov e the sex- and age-specific ov erweight c rite ria defined by the National Health and Examination Surv ey (NHES) percentiles. R ussian b oysshowed comparab le overweight prevalences wi th thatof the U .S . at the 95th percentile of B MI from N HES,w ith prev alences of 11.8 and 11.7 , respectiv ely.

Lower levels o f overwe ight are expe rienced bChina and South Africa, and by girls in China,and South A frica than in the U .S. populationthe 85th percentile is used, the prev alenceweight more than doubles in three of the studytions and becam e m ore com parable to the Ulences. However, in China the majority of ovchildren are concentrated at the 95th percenti

In Table 2 , we present the prevalence rates fstunted and overw e ight. The p ropo rtion o fwho are stunted ranges from 1 5 in Braz il to30.6 among b lack and co lo red South Africdren. In Russia, stunting is a re lative ly new pnon. As show n else whe re , only in the last halw ith the decline in social serv ice s and the p rofree o r very inexpensiv e we aning food , hasemerged as a new nutrition problem (Mroz an1 995, Popk in et al. 1996 ).

A high w e ight-fo r-height is e merg ing as anutrition concern am ong children not onlysam ple countries but elsew here in the lowworld (Monte iro e t al. 1995, Popkin 1994).Thtion of children w ho are ov erw eight in eachvaries from 3.6 in Braz il to 10.4 in China in

The effects of prev ious stunting on presew eight status can be assessed by exam iningratio s in Tab le 2. For child ren in Braz il, the reparently no association betw een stunting anweight-for-height because the risk ratio was 1other countries, s tunted chi ldren have a higheof being overweight: the risk ratios ranged froSouth African children (ei ther black and colortotal population of whites , Asians , blacks , anchildren) to 7.7 am ong R ussians. T here w aseffect of age group on the magnitude of the asbetween stunting and overweight s tatus .

Tab le 3 p re sents the e ffec t o f income contro

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RELATIONSHIP BETW EEN STU NTING A ND O VERW EIG HT 3013

TAB LE 2

T h e relation sh ip betw een stu nted an d overw eigh t statu s

Country , year A ge, y (n)

Prevalence ofstuntedchildren

Prevalence ofoverweight

children

Prevalence o fo ve rw eig ht in

stunted children

Prevalence ofo ve rw e ight in

nonstunted chi ldren

Relat ive riskof overweightbeing stunted

Confidenceinterval( for RR)1

Russia1994/5

China1991

1993

South AfricaTotalBlack and

3-6 (607)7-9 (499)3-9(1106)

3-6(1068)7-9 (687)3-9(1755)3-6 (949)7-9 (688)3-9 (1637)

3-6 (2467)

12.25.69.2

32.426.630.126.724.625.9

28.5

12.26.29.5

8.29.58.7

11.19.6

10.4

7 3

48.635.745.1

17.020.818.322.522.522.4

13.1

7.14.55.9

4.05.44.66.95.46.3

5

6.88.07.7

4.23.94.03.34.23.6

2.6

1 R R = relativ e risk.2 T he relativ e risks for the tw o age groups are not equal.

association betw een stunted and ov erw eight status. Itshould be noted that income may act as a negativeconfounder for that association because w ealth is usually associated, in different directions, w ith stuntingand a high w eight-for-height. C ontrolling for incom e

in this case means essentially to make equal the tw osubg roups of stunted and no n-stunted children regarding access to fo od and also to resources that affect activity lev els of children, the central factors affecting childobesity. Data in Table 3 indicate that incom e controlw as particularly im portant in Braz il rev ealing that inthis country there is also a significant association betw een stunting and overw eight status [relative riskJR R) = 1.7; 1.2-2.3]. Elsew here, w e hav e show n a strongpositive relationship betw een income and a highw eight-for-height in B raz il and also a significant in-

(4.7,9.9)2(4.3, 14.8)(5.6, 10.5)

(2.9, 6.3)(2.5, 6.0)(3.0, 5.4)(2.3, 4.6)(2.7, 6.4)(2.8, 4.7)

(2.0, 3.4)

coloredBrazil3-6(2229)3-6(6237)7-9(4872)3-9(11109)30.616.613.015.07.5

13.04.03.13.63.53.43.55.14.03.13.62.50.91.11.0(1.9, 3.1.2)(0.7,1.3)(0.7,

1.3)

v erse relationship betw een undernutrition and i(M onteiro et al. 1995). How ever, in none of thecountries did income function as a significantfounder or effect m odifier (d ata not show n).

A m easurem ent problem em erges: Is this relship of stunting w ith high w eight-for-height mstatistical artifact resulting from the fact that heon b oth sides of the stunting/ov erw eight relaship? A naly zing the scatter plots and Pearson ctions (not show n) for a linear relationship betw e ight-fo r-height and heig ht-fo r-ag e fo r child ren3-10 y, rev ealed only a slight inv erse relationshitw e en w e ig ht-fo r-height and heig ht-fo r-age fo r altries, w ith a stronger negativ e relationship seenR ussian surv ey. Plo ts and correlations im plied arelationship; how ev er, the inv erse relationship w

TA BL E 3T h e relation sh ip betw een stu ntin g an d overw eigh t statu s: th e eff ects af in cà ³m e adju stm en t f or ch ildren aged

Country,earRussia,

1994/5China19911993South

AfricaTotalBlack

andoloredBrazilUnadjusted

riskratio743221706650Confidencenterval(5.6,

10.5)(3.0,

5.2)(2.7,4.6)(2.0,

3.4)(1.9,3.4)(0.7,

1.3)Adjusted

riskratio7.84.23.52.62.61.7Confidencenterval(5.7,

10.7)(3.1,

5.7)(2.7,4.6)(2.0,

3.5)(1.9,3.4)(1.2,

2.3)

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3014 POPK IN ET A L.

consis tent within height-for-age categories. The Pearson correlation coeff ic ients of weight-for-height witheach height-for-age category revealed that weight-for-height did not vary inversely across all height-for-agecategories, wi th short but no t stunted child ren havingslightly positiv e correlations. Percentages of ov erweight children classified in f ive height-for-age categories revealed a d istinc t U- or inverted J-shaped re lationship between weight-for-height and height-for-agecategories in all countries; that is, the m ajority ofoverweight chi ldren clustered in the lower height-forage Z -score categories. These results also support ab io logical re lationship similar to the U -shap ed re lationship McC ance et al. (1994) observed in which lowand high birth w eight infants w ere at increased riskfor diabetes. T hese results show that the height biasdoes not explain all of the ov erw eight status of ours tudy populat ions , i.e ., tall children do not necessarilyweigh more than short child ren.

DISCUSSION

As no ted earlier, we have no way to validate our useof weight-for-height in these four populations againsta more valid measure o f body fatness. We d id find thatthe estim ate of ov erw eight lev els is low er in C hinawhen sk info lds are used. This ind icates that it is quitepossible that in C hina and our other countries, ov erw eight lev els might be ov erestimated w ith eitherweight-for-height or BMI,and the impact of the associatio n no te d he re should be treated cautiously. In fact,Trowbridge e t al. (1987) examined this topic more systematically among Peruv ian child ren and did not findthat a high weight-for-height associated with stunt ingwas ind icative of obesity.

It is im portant to note that w e are not testing theexac t Barker hypothesis (Barker 1992 and 1994). TheB ark er hypo thesis and o ther b io log ical hy po the sestend to focus on fetal effects . Independent of intrauterine g ro w th re tard ation, many child ren in develo pingcountries, and p oo r child ren in the U .S . and o ther deve loped nations, become stunted during infancy as theresul t of inappropriate weaning practices , repeated infections, and poor d ie t—all in the context of poverty(A dair and G uilkey 1996, Wiecha and Casey 1994).This study presents ev idence of an equally importantrelationship but o ne that we must be cautious in o ver-interpreting without additional animal and epidemio-logical research.

This analy sis has no t contro lled fo r the wide rangeo f fac to rs that affect stunting and may also affect thedeve lopment of overweight. Many of these are b io logical or behav ioral factors that are not ev en m easured(often te rmed unobserved he te rogene ity ). Much morethorough, careful epidemiological research is requiredto confirm these findings.

P ossible m e ch an ism s. A n u m ber of h igh ly stive explanations for the re lationship found bstunting and ov erw eight in children stem frowork of Barker and others (Barker 1992 and 199et al. 1992), and none seem to be m utually excBarker and others propose that hormonal changtheir physiologic responses, such as abdominal

stem from fe tal o r infant undernutrition fac illong -term c hanges base d on metabolic adap(Barker1992,Law et al . 1992).The relationshiper's find ings to stunting is no t straightforward .ever, the extensive explorations of Foge l (1994ways in which he ight, independent of weight arelates to morbidity and mortali ty patterns andgive more re levance to a b io logical hypothesis.ample, stunting during the dev elopmental stafar reaching effects into ad ultho od by inc reasirisk of chronic diseases . Paralle l evidence by Ral. (197 6) sug gests that m etab olic tissues suchhypo thalam us are reprogram m ed as a result omalnutrition during gestation. An inappropriating o f the hypo thalamus, altering appe tite ccould possibly lead to obesity. C learly, a grem ore work is required to exp lo re this topic .

Al ternate reasons for the stunting/obesi ty reship focus on slowed grow th and a changed horesponse in com bination w ith a poor dietaryStunted (chronically malnourished) children halean body mass, result ing in decreased basal merate and physical ac tiv ity. W hen energy intakequate, w e see a d iffe rence in line ar g rowth pov s. deposition of adipose tissue (B arac-N ietoTrowbridge 1983).This may occur for a numbersons: 1 ) the diet is lim ited in essential nutrienquired fo r linear gro wth but no t fo r an inc reasepose tissue/ and 2} early nutritional programmiresult in a number of hormonal e ffects such thatg row th is lim ited, but potential fo r we ight gainIn the past, stunting and access to food w ereassociated, but that linkage m ay not be as apnow in countries undergoing the nutrition trans

Little systematic c linical research has been dthe s tunting period and its subsequent re lationsobesity. O thers hav e linked m ultiple other cainfant obesity such as bottle feeding, and infantitself, w ith subsequent obesity, but they havlooked another cause , the stunted child (see Poal. 1986 ). Serdula and o the rs (1 99 3) have showtionships betw een child obesity for a v arietyand subsequent obesity.

The results of our research and prev ious liteare generaliz able to a w ide range of populatioenvironments. Research among U.S. Hispanicse t al. 1994), Jamaican child ren (Forreste r e t al.and others found some of the same bio logical rship s as did Bark er (1 992). Research on stuntinoverweight seems most common among Hispaulations . Mexican-American children are more

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to be short and ov erw eight (M alina et al. 1986, M artor-ell et al. 1987 , Z av aleta and M alina 198 0). O ther ethnicgroups in the U.S., particularly the Hm ong, a Laotianim migrant group, are experiencing increasing obesityw hile also m anifesting high lev els of stunting. By age4 y, close to 25 of a sam ple of Hm ong children liv ingin Minnesota w as stunted and by that same age over

22 w ere ov erw eight (Him es et al. 1992).W hy have researchers not found this pattern ofstunting and obesity at earlier periods of history w henhigh rates of stunting also existed? The m ost logicalreason is that the underly ing social and econom ic circumstances that caused the high level of stunting didnot provide the basis for obesity to em erge as a publichealth concern. W hy w ith the v ery large distributionof low birth w eight status in low er incom e countries,and the v ery high incidence of stunting, do w e not hav em ore obesity ? It m ight be as sim ple as stating that therehas been a lack of research on this issue: researchersinterested in stunting w ere focused on problem s of infectious diseases and undernutrition and not w orriedabout obesity. Or it is possible that the biological andbehav ioral adaptations associated w ith stunting w ereim portant and that the underly ing food, disease, andsocioeco nom ic conditions that caused stunting continued to affect the liv es of these children. In other w ords,poor socioeconomic conditions did not allow for theexpression of obesity in the population. T he nutritiontransition w ith the rapid shift in the composition ofdiet and activ ity patterns prov ides the conditions forthe complications of stunting to emerge. Further research is required to unrav el this speculatio n.

M ore importantly , the vast set of econom ic and dem ographic changes occurring in m any low er incom eand m iddle incom e countries ov er the past few decadescreates an entirely new set of circumstances for thefuture. There is m inim al opportunity for leisure activity in m any areas, and large changes in transpo rtationand w ork are beginning to require much less energyexpenditure. Elsew here, w e dem onstrated these activity pattern changes for Chinese adults (Popkin 1994).There are few data to show if these same trends w illoccur fo r child ren. Concurrent changes in the structureof diet are rapid. A higher fat and low er carbohy dratediet is rep lacing the trad itional one in m any countries.

T he result is a significant change in body com positionam ong all age groups as w as dem onstrated in Thailand(L adda et al. 1993).

M ore research is being undertaken on all aspects ofchild stunting , b ut there are s till few serio us initiativesto develop the range of public health programs to reduce infant nutrition insults (e.g., im prov em ent of infant w eaning foods). It is important to point out thatif the program ming hy pothesis (B arker 1992 and 1994)is prov ed to be correct, a m ajor w eapon against chronicdiseases is this im provement of maternal and infantnutrition. The rapid increase in stunting in R ussia follow ing the econom ic reform s and dism antling of parts

of a m aternal and child health nutrition programvides an example of the importance of publicprograms or lack thereof in addressing this co(M roz and Pop kin 1995). We hope the future w illm ore aggressiv e w ork on this m ost com plex prW hat w e do know is that there are conditionsw hich stunting m ig ht b e rev ersed am ong older c

and adolescents, but there is little evidence inincome countries to show that w e are reversi(A dair and G uilkey 1996, M artorell et al. 1994)over, if stunting w ere to be reversed, w e do notthat the m etabolic changes B ark er and others hysize to be related w ith grow th retardation w illversed. That is, w e cannot answ er the questiow hether children w ho face stunting w ill grow ua special biological v ulnerability and thus if thoption is to reduce insults during pregnancy afancy.

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