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The Association Between Diet and Height in the Post-Infancy Period Changes With Age and Socioeconomic Status Among Filipino Youths

The Association Between Diet and Height in the Post-Infancy Period Changes With Age and Socioeconomic Status Among Filipino Youths

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Community and International Nutrition
The Association between Diet and Height in the Postinfancy PeriodChanges with Age and Socioeconomic Status in Filipino Youths
1
Cara L. Eckhardt,
2
Chirayath Suchindran,* Penny Gordon-Larsen,
and Linda S. Adair
Food Consumption and Nutrition Division, International Food Policy Research Institute, Washington, DC andDepartments of *Biostatistics and
Nutrition, University of North Carolina at Chapel Hill, Chapel Hill, NC
 ABSTRACT Whether the determinants of linear growth can have independent effects beyond the critical infancyperiod has been questioned. This research uses uniquely suited data from
2000 youths from the Cebu Longi-tudinal Health and Nutrition Study in the Philippines to examine the association between diet and height in thepostinfancy period. Anthropometric, diet, and other data were collected bimonthly from 0 to 2 y, and at the meanages of 8, 11.5, 15.5, and 18.5 y. Generalized Estimating Equations were used to quantify the mean effects of dietdiversity and energy intake on height across increments demarcated by the postinfancy data (2–8.5, 8.5–11.5,11.5–15.5, and 15.5–18.5 y). We examined whether the effects differed by socioeconomic status (SES) and age.Effects with
P
0.05 were considered significant. Each additional unit of diet variety (range 0–8 U) was associatedwith a significant 0.33-cm increase in height in boys. Each additional 100 kcal (4186 kJ) was associated withsignificant increases in height of 0.05 cm in boys, and 0.02 cm in girls. Significant interactions ( 
P
0.15) with SESshowed that each 100 kcal increase in energy intake was associated with a 0.08-cm increase in height at low SESwith no difference at high SES. In both boys and girls, the effects of energy intake decreased with age, as shownby a significant age interaction ( 
P
0.15). The methods used incorporate the longitudinal nature of the data to offera unique examination of the association between diet and height in the postinfancy period. J. Nutr. 135:2192–2198, 2005.KEY WORDS:
diet diversity 
energy intake
height
linear growth
developing country 
Diet is arguably the most influential determinant of lineargrowth because it is through diet that the influences of otherdeterminants of linear growth such as socioeconomic status(SES)
3
and infection are largely played out (1–4). Under-standing the association between diet and linear growth isparticularly salient in developing countries. In these areas,linear growth retardation affects
30% of children, with muchhigher proportions affected in some areas (5); it is also accom-panied by increased morbidity and mortality (6,7) and a vari-ety of other poor outcomes (8–13).Research on the association between diet and linear growth indeveloping countries thus far has been constrained largely to theeffects seen during infancy and early childhood for several reasons(14–22).Lineargrowthretardationtendstomanifestitselfduringthe1st2yoflifebecauseinfancymarkstheperiodoffastestlineargrowth velocity and is particularly vulnerable (23). Thus, re-search has focused on this important period, and has questionedwhether growth trajectories thereafter are capable of improve-mentandwhetherdeterminantsofheightcanhavefurthereffectsthat are independent of their influence during infancy. In addi-tion, due to the difficulties of collecting longitudinal diet andother data in developing countries, there are no studies to datethat have had sufficient data to comprehensively examine dieteffects over the entirety of the postinfancy period through theattainment of adult stature.We examined the association between diet and height inthe postinfancy period using data from the Cebu LongitudinalHealth and Nutrition Survey (CLHNS), which provided lon-gitudinal data on a variety of anthropometric and other mea-sures from birth through adult stature. Most studies of diet andlinear growth have focused on macronutrient intakes or onspecific micronutrients or foods despite the fact that intakes of macronutrients and micronutrients are associated and worktogether to influence stature (24). We examined the effects of both energy intake and diet variety (DV), a broad indicator of micronutrient adequacy and a measure that allows for com-parisons to be made across the entirety of the postinfancyperiod given the types of diet data collected at the variousCLHNS survey points.Using longitudinal data analysis methods, we determinedthe magnitude of the mean independent effects of diet onheight across the postinfancy period; second, we examinedwhether these effects were expressed differently depending onSES and accompanying levels of need; and last, we determinedhow the observed effects of diet in the postinfancy perioddiffered with age.
1
Presented at Experimental Biology 2005, April 2005, San Diego, CA [Eck-hardt, C. L., Suchindran, C., Gordon-Larsen, P. & Adair, L. S. (2005) Therelationship between diet and height is enhanced at low SES and decreases withage among Filipinos in the post-infancy period. FASEB J. 19: #10548 (abs.)].
2
To whom correspondence should be addressed.E-mail: c.eckhardt@cgiar.org.
3
 Abbreviations used: CLHNS, Cebu Longitudinal Health and Nutrition Sur-vey; DV, diet variety; GEE, generalized estimating equation; HAZ, height-for-ageZ-score; SES, socioeconomic status.
0022-3166/05 $8.00 © 2005 American Society for Nutritional Sciences.Manuscript received 13 November 2004. Initial review completed 2 January 2005. Revision accepted 7 July 2005.
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SUBJECTS AND METHODS
Study population and design.
Data come from the CLHNS, acommunity-based cohort study of children born in 1983–1984 inurban and rural communities of Metro Cebu, the most rapidly grow-ing metropolitan area of the Philippines. The CLHNS data providedetailed longitudinal anthropometric, diet, and household SES dataalong with measures of maturational timing and other factors relatingto maternal and child health.Data collection for the first round of the CLHNS began during thelast trimester of pregnancy for all participating mothers. All pregnantwomen living in the selected communities during the enrollmentperiod were invited to participate, and
95% enrolled. In the firstround of the survey (1983–1986), 3080 singleton live births wereincluded. Child data were collected at birth and then bimonthly for2 y. Follow-up surveys took place in 1991 (mean age 8.5 y) with 2264children (74% of the original sample), in 1994 (mean age 11.5 y)with 2192 children (71% of the original sample), in 1998 (mean age15.5 y) with 2089 children (68% of the original sample), and in 2002(mean age 18.5 y) with 2029 children (66% of the original sample).Data were collected in accordance with protocols approved by theInstitutional Review Board of School of Public Health at the Uni-versity of North Carolina at Chapel Hill. Of the 572 subjects whowere lost to follow-up during the initial survey, 155 were lost due todeath (27%), whereas the rest were not found or were no longerliving in Metro Cebu. Of the 244 subjects lost between the end of theinitial survey and the 1991 follow-up, 55 died (23%). The remaininglosses in this and subsequent periods were attributable primarily tomoving outside of the Metro Cebu study area. In the longitudinalmodels described below, these data contribute 4047 observations inboys and 3656 observations in girls.
 Anthropometric measures.
During the initial study period (frombirth through 2 y of age), recumbent length was measured to thenearest millimeter using a custom-designed length measuring board.During the follow-up surveys, standing height was measured using aportable stadiometer. All measurements were performed in the chil-dren’s homes by trained project personnel using standard techniques.Maternal height was measured at baseline using the same techniques.Height-for-age Z-scores (HAZ) were calculated using the lambda,mu, and sigma parameters (the power transformation, median, andCV, respectively, from the Box-Cox transformation) from the 2000CDC growth reference data (25,26). The new references were chosenbecause they are more appropriate for breast-fed children and becausethey provide reference data past 18 y of age, which is necessary forcalculating HAZ from the 2002 CLHNS follow-up.
 Maturational timing.
Timing of sexual maturation was assessedby questionnaire using age at menarche in girls and pubic hair stagein boys. Girls were asked their age at menarche at each follow-upsurvey from age 11.5 y on. Pubic hair development was self-assessedby having boys compare themselves to line drawings depicting the 5Tanner stages of development (27) at both 15.5 and 18.5 y of age andwas validated against physician assessment in a separate but similarsmall sample that was recruited for that purpose. For ease of analysis,and because there were few subjects at the extremes, pubic hairdevelopment was categorized as early (Tanner stages 4 and 5), aver-age (Tanner stage 3), and late (Tanner stages 1 and 2) based on the1998 survey data at mean age 15.5 y.
SES index.
The SES index used was developed for the Cebu data,and reflected 3 facets of SES, i.e., income, assets, and maternaleducation. One point was awarded for ownership of each of 4 assets:air-conditioning, television (color or black and white), refrigerator, orvehicle (car, bus, truck, or motorized tricycle). Additionally 1, 2, or3 points were awarded in concordance with falling into the lowest,middle, or highest tertile of per capita income, respectively. Last, 1point was awarded if the mother had completed primary school, and2 points were awarded if the mother had any schooling beyondprimary school. Thus, the SES index has a potential range of 0–9points. The outcome data in the longitudinal models used and de-scribed below are height measures at 8.5, 11.5, 15.5, and 18.5 y of age.We used the mean SES index from survey points 2 and 8.5, 8.5 and11.5, 11.5 and 15.5, and 15.5 and 18.5 y of age, respectively, aspredictor variables relating to these outcomes to better describe themean SES influences experienced by the subjects between surveysand leading up to the outcome measures included.
Diet variety.
We include a DV score in our models because manymicronutrients are important for supporting linear growth, yet intakesof micronutrients are highly correlated, making it difficult to examinetheir independent effects. The literature shows that DV is associatedwith overall nutrient adequacy, making it a useful measure of dietquality (28–30).Because several nutrients important for growth (such as zinc)cannot be isolated from the Cebu data because they are not includedin the Philippine food composition tables (31), we used a foodgroup–based DV index, a common approach (28–30,32–34), ratherthan a nutrient-based index. We based our score on a DV scorecreated previously for the Cebu population (35) in which 1 point wasawarded for having eaten at least 1 food from each of several cate-gories: fish, animal source foods, staple cereals, other starches, vege-tables, fruits, beans and nuts, and dairy.A variety of dietary assessment tools were used during the Cebustudy. An FFQ covering a recall period of 1 y was administered at8.5 y of age, one 24-h recall was administered at 11.5 y of age, and two24-h recalls were administered on nonconsecutive days at each of thesurvey points thereafter. Portion sizes for both the FFQ and the 24-hrecalls were ascertained using the same set of field-tested food modelsat each survey point. Mothers or guardians were the respondents forthe children through age 11.5 y, whereas the subjects responded forthemselves thereafter. The differences between the dietary assessmenttools used imposed some difficulties in creating comparable measuresof dietary variety over time. The FFQ is preferable for representingusual intake (36), but because it reports intakes based on a compre-hensive list of 77 foods, it is likely to show greater dietary variety thanthe 24-h recalls. For the 24-h recall data, greater variety would likelybe reflected through the use of data from two 24-h periods (at ages25.5 and 18.5 y) than from one 24-h period (at age 11.5 y). Inaddition, 24-h recalls may not represent usual intake patterns (37).An additional independent set of questions was administered inthe same way at each time point, listing what foods were usually eatenfor breakfast, lunch, dinner, and snacks. Thus, we used the responsesfrom these “usual intake” questions to construct a comparable DVscore at 8.5, 11.5, 15.5, and 18.5 y of age with a possible range of 0to 8 points. Mendez (35) demonstrated the validity of this methodwithin the Cebu data by validating the DV score constructed fromthese additional “usual intake” questions against the nutrient intakedata from the more standard 24-h recall data at 11.5 y of age, andfound that the DV score was strongly associated with nutrient ade-quacy for a variety micronutrients such as iron, calcium, and vitaminA (35).
 Energy intake.
We use kilocalories (kcal)
4
per day as calculatedfrom the FFQ at 8.5 y of age and from the 24-h recalls at the latersurvey points, recognizing that the energy intakes are likely to besomewhat inflated at 8.5 y of age but that the association betweenincreases in intake and increases in height is assumed to be the same.The use of energy tertiles (to overcome the differences due to thediscrepancies in methods) did not substantively change our findings;thus we used the continuous measure energy intake from 8.5, 11.5,15.5, and 18.5 y of age.
Statistical analysis.
Frequencies and percentages for matura-tional timing in boys, and means and SD for height, HAZ, SES index,DV score, and energy intake for each survey point from which theheight outcome measures are taken (ages 8.5, 11.5, 15.5, and 18.5 yof age) were determined. Means and SD for height and HAZ at 2 yof age were also calculated because height at 2 y is included in ourmodels as a control. Although the HAZ data were not used in ourmodels, they are provided to show the extent of linear growthretardation in the Cebu population.We fit a longitudinal model using Generalized Estimating Equa-tions (GEE) predicting height (using outcome data from 8.5, 11.5,15.5, and 18.5 y of age). We selected this type of “population average”regression model because we were not interested in estimating sub-ject-specific parameters. GEE models also account for correlations of 
4
1 kcal
4.186 kJ.
DIET AND HEIGHT IN FILIPINO YOUTH
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repeated measures within individuals, allow for unequally spacedlongitudinal measures, and maximize sample size and power by ac-commodating missing observations (38).We modeled the mean effects of several time-varying and non-time-varying predictors on height across the postinfancy growth pe-riod. Thus, the outcome measure of height comes from 8.5, 11.5, 15.5,and 18.5 y of age. The time-varying predictors included our mainvariables of interest, i.e., DV and energy intake. The time-varyingcontinuous SES index variables were also included to control forconfounding in the diet/growth association because SES likely affectsfood availability and quality, and also has effects on growth via factorssuch as morbidity and access to health care. The diet variables weretaken from the same survey from which the outcome was drawnrather than using mean values between survey points, as was donewith the SES data. Because the surveys were spaced several yearsapart and energy needs and diet change significantly during child-hood, concurrent diet was considered to be a more accurate repre-sentation of recent diet affecting height than a mean measure. Ageand age-squared variables were also included to account for thenonlinear association between age and height.The non-time-varying predictors included mother’s height as aproxy for genetic influences and generational effects, maturationaltiming, and height at 2 y of age. Maturational timing variables (ageat menarche for girls and pubic hair development stage at age 15.5 forboys) were included because although these variables refer specificallyto events that occur in puberty, they reflect developmental trajecto-ries that begin much earlier and which may influence the tempo of growth-attained stature. Height at 2 y of age was included to controlfor height at the onset of the postinfancy period and to control for theeffects of diet and other predictors of growth during infancy, thusallowing our models to focus on independent postinfancy effects.Lowess smoothers (39) were used to identify any gross violationsof the linearity assumption between the dependent and independentvariables for each survey point. Three boys with energy intakes
6000 kcal/d (1 at 15.5 y of age and 2 at 18.5 y of age) were excludedfrom the analysis because their reported intakes were consideredimplausible and because they were identified as outliers in the height/energy intake association.Interactions between the SES index and both the DV and theenergy intake variables were explored to determine whether individ-uals of low SES might be more responsive to dietary improvements.Interactions of both the DV and the energy intake variables with theage and age-squared terms were tested to determine whether theassociations between the diet variables and linear growth varied withage.Coefficients with
P
0.05 were considered significant for maineffects, whereas
P
0.15 was considered significant for interactionterms. All analyses were performed in Stata for Windows (Release8.0, Stata Corporation).
RESULTS
Descriptive statistics.
The mean HAZ was below thelevel of stunting (less than
2.0) at ages 2 and 8.5 y in bothboys and girls with some recovery from stunting thereafter(
Table 1
). The mean HAZ measures at 18.5 y, which likelyreflect final stature for the majority of the population, wereabove, although still near the cutoff point indicating stunting.These data thus indicate widespread linear growth retardation,with some improvements with age, in the Cebu population.The SES indices improved in both boys and girls over time,reflecting the rapid modernization and economic developmentoccurring in the Philippines. The DV scores remained rela-tively stable over time in both boys and girls, whereas energyintake data showed inflated intakes at age 8.5 y (due to the useof a FFQ at this survey point as opposed to the 24-h recalls atthe other survey points) with increasing intakes in both boysand girls from 11.5 to 18.5 y of age.
 Mean dietary effects in the postinfancy period.
The co-efficients and SE from the main effects models, without inter-action terms included, are shown in
Table 2
. Energy intakeand mother’s height were positively associated with height inthe postinfancy period in both boys and girls. The coefficientfor DV was positive and significant in boys, whereas there wasvirtually no DV effect seen in girls. Early maturation wasassociated with greater height in boys and girls as seen by thepositive significant coefficient for the early maturation variablein boys and by the significant negative association between ageat menarche and height in girls.
Interactions between SES and the diet variables.
Al-though the mean daily energy intake tended to rise with SESindex level at each age (as would be expected), there wassufficient overlap of energy/intake among SES levels to merittesting interactions between energy intake and SES. Thecorrelation between kcal/d and the SES index was
0.40 atages 8.5 and 11.5 and weakened thereafter. Diet variety alsotended to rise with SES at young ages, with a correlation of 0.35 at age 8.5, but the correlation was very weak by age 18.5(
0.10). Interactions of both DV and energy intake with thecontinuous variable SES index were tested. In both boys andgirls, only the interactions with energy intake were significant(
P
0.15) and were retained in the models with results shownin
Table 3
. To better understand the potential magnitude of this effect in the Cebu population, we used the model coeffi-
TABLE 1
Characteristics of study participants
1
Boys GirlsMother’s height,
cm
150.64
5.00 150.47
5.00 Age at menarche in girls,
13.12
1.04Maturational timing in boys,
2
%
Early 41.1 Middle 38.3 Late 20.7 Child height,
cm
2 y 79.90
3.56 78.34
3.618.5 y 117.74
5.54 117.63
5.5711.5 y 132.39
7.04 135.36
7.5915.5 y 158.47
6.78 149.02
5.5218.5 y 162.63
5.89 151.00
5.45Child HAZ2 y
2.14
1.00
2.16
1.028.5 y
2.28
0.99
2.25
1.0211.5 y
1.99
0.98
1.68
0.9915.5 y
1.91
0.81
1.98
0.8618.5 y
1.92
0.81
1.88
0.84SES index8.5 y 4.45
2.17 4.34
2.0511.5 y 4.84
2.40 4.80
2.3115.5 y 5.10
2.34 5.00
2.2918.5 y 5.41
2.33 5.34
2.23DV score8.5 y 4.74
1.40 4.72
1.3211.5 y 4.20
0.96 4.30
0.9515.5 y 4.63
0.99 4.50
0.9018.5 y 4.56
0.97 4.60
0.92Energy intake,
3
 kcal/d
8.5 y 1506
600 1354
50611.5 y 1257
612 1140
51415.5 y 1915
774 1287
55618.5 y 2315
920 1777
762
1
Descriptive statistics for maturational timing in boys are means
SD or %.
2
Tanner pubic hair development stages at age 15.5 were used tocategorize boys as early
stages 4 or 5, middle
stage 3, and late
stages 1 or 2.
3
1 kcal
4.186 kJ.
ECKHARDT ET AL.
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